Frank-Starling Relationship
2002; Lippincott Williams & Wilkins; Volume: 90; Issue: 1 Linguagem: Inglês
10.1161/res.90.1.11
ISSN1524-4571
AutoresRichard L. Moss, Daniel P. Fitzsimons,
Tópico(s)Cardiac electrophysiology and arrhythmias
ResumoHomeCirculation ResearchVol. 90, No. 1Frank-Starling Relationship Free AccessEditorialPDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessEditorialPDF/EPUBFrank-Starling RelationshipLong on Importance, Short on Mechanism Richard L. Moss and Daniel P. Fitzsimons Richard L. MossRichard L. Moss From the Department of Physiology and the Cardiovascular Research Center, University of Wisconsin Medical School, Madison, Wis. and Daniel P. FitzsimonsDaniel P. Fitzsimons From the Department of Physiology and the Cardiovascular Research Center, University of Wisconsin Medical School, Madison, Wis. Originally published3 Apr 2018https://doi.org/10.1161/res.90.1.11Circulation Research. 2002;90:11–13The Frank-Starling relationship is an intrinsic property of myocardium by which increased length (or ventricular volume) results in enhanced performance during the subsequent contraction.1–3 This relationship appears to be very important in cardiac function because increased venous return and the corresponding increase in end-diastolic volume result in greater stroke volume during the next beat. The ventricles can thus accommodate increased venous return by means of a more vigorous contraction that ejects the greater volume of blood from the heart.Although the physiological significance of the Frank-Starling relationship is widely appreciated, its cellular basis is not well understood. One hypothesis is that more cross-bridges interact with actin at longer sarcomere lengths due to length-dependent reductions in lateral spacing between thick and thin filaments,3–5 ie, due to closer proximity to actin more crossbridges bind and thereby increase contractile force (see Figure). Measurements in permeabilized myocardium held at constant length have shown that osmotic compression increases force at each [Ca2+]. Thus, the greater Ca2+ sensitivity of force at long lengths can be achieved at short lengths by reducing fiber diameter. Moreover, osmotic compression actually eliminates the length dependence of Ca2+ sensitivity.4 This evidence suggests that lateral filament spacing is a primary determinant of the Frank-Starling relationship, but the evidence is incomplete because studies to date have only measured muscle diameter and not the actual spacing between thick and thin filaments. Diameter and filament separation are likely to increase or decrease in concert, but these changes need not be proportionate because the shape of the muscle cross section can change with stretch or with osmotic compression. Until now, no one has quantified the lateral spacing of thick and thin filaments in such experiments due to the technical difficulty of the measurements. Download figureDownload PowerPointMyocardial sarcomere and myofilaments. A, Diagram of the sarcomere showing approximate spatial relationships of thick and thin filaments and putative interactions of titin with the filaments, which would give rise to radial and axial restorative forces when the sarcomere is stretched.11 B, Diagram of the thick and thin filaments illustrating the decrease in lateral separation at long lengths. The probability of crossbridge interaction increases at long lengths due to closer proximity to actin.In this issue of Circulation Research, de Tombe and colleagues6 report results of studies in which x-ray diffraction was used to quantify the lateral spacing of thick and thin filaments in cardiac muscles in which force and length were also measured. The regular structure of the sarcomere produces an x-ray diffraction pattern that reports the lateral spacing between thick and thin filaments, ie, filament lattice spacing. As sarcomere length is increased, lattice spacing decreases and vice versa. The authors assessed force as functions of length and lattice spacing, and using osmotically active compounds, they were able to independently vary lattice spacing and length. To the authors' great credit, such experiments are technically demanding and have yielded results that could profoundly influence current thinking.Length-Dependent Variations in Force Can Occur With No Changes in Filament Lattice SpacingInitial experiments by Konhilas et al6 reproduced important features of earlier work, ie, increases in muscle length or osmotic compression of skinned preparations were found to increase Ca2+ sensitivity. However, they found no effect of osmotic compression on the length dependence of Ca2+ sensitivity, which contrasts with an earlier report5 in which compression eliminated the length dependence. The authors suggest that the difference may be related to differences in species used, but they have not eliminated the possibility that there are unrecognized systematic differences in methods.Using x-ray diffraction, Konhilas et al6 found that filament lattice spacing decreased when the muscle was stretched or osmotically compressed with dextran, which was the expected result. However, they found that dextran compressed muscle diameter to a greater extent than interfilament lattice spacing, ie, earlier studies overestimated the degree of lattice compression from measurements of muscle diameter. The most important results were as follows: (1) lattice compression with dextran tended to reduce the stretch-dependent decrease in filament lattice spacing, but had no significant effect on the length dependence of Ca2+ sensitivity of force; and (2) osmotic compression to achieve lattice spacings typical of a longer length produced no change in Ca2+ sensitivity of force. These results are not easily reconciled with models in which filament lattice spacing is the sole determinant of the length dependence of Ca2+ sensitivity and at the very least suggest that other mechanisms are involved.Given the technical difficulty of these measurements, consideration needs to be given to experimental uncertainties. In this regard, sarcomere length was not actually measured during contraction, at least at higher levels of activation, due to disappearance of the diffraction pattern. The inability to consistently measure active sarcomere length reduces confidence in the quantitative relationships between Ca2+ sensitivity or lattice spacing and length, but does not detract from the main finding of the paper, ie, osmotic compression of lattice spacing at short length to achieve the smaller lattice spacing at a long length does not mimic the greater Ca2+ sensitivity observed at the longer length.Another important issue, studied previously by this group,7 is that skinning of cardiac muscle results in swelling of diameter by about 20%, ie, filament lattice dimensions are greater in skinned than in living preparations. In view of this, the experiments here were likely done at greater than normal filament lattice spacings, although the degree of swelling is not evident from the results, nor is it possible to know whether swelling influenced the results. A puzzling aspect of the results is that compression reduced the length-dependent variations in filament lattice spacing, and yet, living preparations with much smaller lattice dimensions exhibit substantial length dependence of lattice spacing.7 This gives rise to a concern in this and previous studies, voiced by Konhilas et al,6 that the use of high molecular weight polymers might have nonspecific effects on the filament lattice in addition to osmotic compression. To investigate this possibility, new methods are needed for altering filament lattice spacing without osmotically active polymers.The Mechanism of the Frank-Starling RelationshipThe work by Konhilas et al6 has important implications for ultimate understanding of the mechanism(s) underlying the Frank-Starling relationship. They show that osmotic compression that is sufficient to mimic the change in filament lattice spacing observed when resting sarcomere length is increased did not significantly change the Ca2+ sensitivity of force. The conundrum now is that others have been able to mimic the length-dependent changes in Ca2+ sensitivity only by changing fiber diameter,3–5 ie, other than muscle length, lattice spacing is the sole geometrical perturbation that alters Ca2+ sensitivity. Konhilas et al6 suggest a useful way to consider the role of lattice spacing: "… the interfilament spacing theory must be amended to include a variable impact of myofilament lattice spacing on myofilament Ca2+ sensitivity, depending on the overall extent of compression of the myofilament lattice" (page 63).In view of the present results, other mechanisms must contribute to the length dependence of Ca2+ sensitivity. One possibility is that the number of interacting crossbridges changes with muscle length due to the change in overlap of thick and thin filaments. However, based on the relatively narrow length range in which myocardium operates and the large changes in submaximal forces seen in myocardium over this range, this mechanism would make only minor contributions to length-dependent contraction.1,2 Another idea is that crossbridge binding to actin increases the affinity of Ca2+ binding to the regulatory protein troponin. Results show that this is indeed the case,8 but it is still unclear whether increased Ca2+ binding is mainly a result of crossbridge binding or if increased Ca2+ binding in turn recruits additional crossbridges to the thin filament and increases force.3Two other mechanisms might contribute to the length dependence of Ca2+ sensitivity in myocardium, with or without length-dependent changes in filament lattice spacing.Cooperation in Crossbridge BindingThe increase in Ca2+ sensitivity at stretched lengths may involve positive cooperativity in crossbridge binding to actin, ie, initial crossbridge binding facilitates further binding that in turn increases force at any given [Ca2+]. Consistent with this idea, bathing skinned myocardium with a strong-binding derivative of myosin substantially reduces the length-dependent changes in Ca2+ sensitivity of force.9 Presumably, application of the strong binding derivative more nearly saturates the cooperativity of crossbridge binding, so that the activation of force does not vary as much with muscle length. The mechanism of increased cooperativity at long lengths might be due to increased probability of initial crossbridge binding to actin due to reduced lattice spacing or an effect of stretch on crossbridge disposition (below).Strain of Elastic ProteinsDecreased strain of the elastic protein titin reduces the length dependence of Ca2+ sensitivity of force in myocardium.10–12 Granzier and colleagues11 interpreted their results with a lattice spacing model, ie, a component of titin stress is directed radially rather than axially, so that increased resting force at long lengths would actually pull the thick and thin filaments closer together and increase the likelihood of crossbridge binding to actin (Figure). This is a potentially important idea and is testable with x-ray methods described by Konhilas et al.6 Another possibility is that titin strain alters myosin packing in the thick filament or the orientation of myosin heads along the thick filament backbone. If such changes contribute to increased Ca2+ sensitivity of force at long lengths, the contribution would be eliminated by a reduction in titin strain, which is what has been observed.11,12 These ideas need to be tested quantitatively to address the underlying mechanisms. First, is the effect of titin strain on Ca2+ sensitivity of force observed in skinned myocardium with expanded filament lattice spacing still present at physiological lattice spacing? This question could be studied by assessing effects of titin strain on contraction at compressed lattice dimensions typical of intact myocardium at long and short working lengths. Second, are there changes in cross-bridge disposition at long lengths that might increase the likelihood of crossbridge binding to actin? Assessment of meridional reflections and off-layer layer lines in the x-ray pattern would help resolve this issue.SummaryKonhilas et al6 have provided a much needed quantitative test of the idea that changes in filament lattice spacing account for the increase in Ca2+ sensitivity of myocardial force at long lengths. Their results imply that length-dependent changes in lattice spacing are not the only factor, and possibly not the principal factor, determining the length dependence of Ca2+ sensitivity thought to underlie the Frank-Starling relationship. At the same time, their findings do not suggest a mechanism to explain length-dependent activation in myocardium. Possibilities include effects of stretch on thick filament structure or cross-bridge disposition via the elastic protein titin or length-dependent changes in cooperative processes that modulate activation, but such ideas need to be explored. In this regard, the x-ray methods used by Konhilas et al6 have extraordinary potential for elucidating effects of stretch on the structure of the myofilaments, but such experiments will be even more difficult than those discussed here. The emerging complexity of mechanisms underlying the Frank-Starling relationship recalls the words of A.V. Hill: "There are more things in heaven and earth, Horatio, … and even in … [heart] muscles" (page 22).13The opinions expressed in this editorial are not necessarily those of the editors or of the American Heart Association.FootnotesCorrespondence to Richard Moss, Dept of Physiology, 1300 University Ave, Madison, WI 53706. E-mail [email protected] References 1 Allen DG, Kentish JC. The cellular basis of the length-tension relation in cardiac muscle. J Mol Cell Cardiol. 1985; 17: 821–840.CrossrefMedlineGoogle Scholar2 Lakatta EG. Length modulation of muscle performance: Frank-Starling law of the heart.In: Fozzard HA, ed. The Heart and Cardiovascular System. New York, NY: Raven Press Publishers; 1992:1325–1351.Google Scholar3 Fuchs F, Smith SH. Calcium, cross-bridges, and the Frank-Starling Relationship. News Physiol Sci. 2001; 16: 5–10.MedlineGoogle Scholar4 McDonald KS, Moss RL. Osmotic compression of single cardiac myocytes eliminates the reduction in Ca2+ sensitivity at short sarcomere length. Circ Res. 1995; 77: 199–205.CrossrefMedlineGoogle Scholar5 Fuchs F, Wang Y-P. Sarcomere length versus interfilament spacing as determinants of cardiac myofilament Ca2+ sensitivity and Ca2+ binding. J Mol Cell Cardiol. 1996; 28: 1375–1383.CrossrefMedlineGoogle Scholar6 Konhilas JP, Irving TC, de Tombe PP. Myofilament calcium sensitivity in skinned rat cardiac trabeculae: role of interfilament spacing. Circ Res. 2002; 90: 59–65.CrossrefMedlineGoogle Scholar7 Irving TC, Konhilas JP, Perry D, Fischetti R, de Tombe PP. Myofilament lattice spacing as a function of sarcomere length in isolated rat myocardium. Am J Physiol. 2000; 279: H2568–H2573.Google Scholar8 Hofmann, PA, Fuchs F. Bound calcium and force development in skinned cardiac muscle bundles: effect of sarcomere length. J Mol Cell Cardiol. 1988; 20: 667–677.CrossrefMedlineGoogle Scholar9 Fitzsimons DP, Moss RL. Strong binding of myosin modulates length-dependent Ca2+ activation of rat ventricular myocytes. Circ Res. 1998; 83: 602–607.CrossrefMedlineGoogle Scholar10 Carzola O, Vassort G, Garnier D. Length modulation of active force in rat cardiac myocytes: is titin the sensor? J Mol Cell Cardiol. 1999; 31: 1215–1227.CrossrefMedlineGoogle Scholar11 Cazorla O, Wu Y, Irving TC, Granzier H. Titin-based modulation of calcium sensitivity of active tension in mouse skinned cardiac myocytes. Circ Res. 2001; 88: 1028–1035.CrossrefMedlineGoogle Scholar12 Fukuda N, Sasaki D, Ishiwata S, Kurihara S. Length dependence of tension generation in rat skinned cardiac muscle. Circulation. 2001; 104: 1639–1645.CrossrefMedlineGoogle Scholar13 Hill AV. First and Last Experiments in Muscle Mechanics Cambridge University Press; 1970.Google Scholar Previous Back to top Next FiguresReferencesRelatedDetailsCited By Kampourakis T and Irving M (2021) The regulatory light chain mediates inactivation of myosin motors during active shortening of cardiac muscle, Nature Communications, 10.1038/s41467-021-25601-8, 12:1, Online publication date: 1-Dec-2021. Tamargo M, Nash T, Fleischer S, Kim Y, Vila O, Yeager K, Summers M, Zhao Y, Lock R, Chavez M, Costa T and Vunjak-Novakovic G (2021) milliPillar: A Platform for the Generation and Real-Time Assessment of Human Engineered Cardiac Tissues, ACS Biomaterials Science & Engineering, 10.1021/acsbiomaterials.1c01006, 7:11, (5215-5229), Online publication date: 8-Nov-2021. de Souza T, Giatti M, Nogueira R, Pereira R, Soub A and Brandão M (2020) Inferior Vena Cava Ultrasound in Children, Pediatric Critical Care Medicine, 10.1097/PCC.0000000000002240, 21:4, (e186-e191), Online publication date: 1-Apr-2020. Saghiv M and Sagiv M (2020) Cardiovascular Function Basic Exercise Physiology, 10.1007/978-3-030-48806-2_6, (285-369), . Izu L, Kohl P, Boyden P, Miura M, Banyasz T, Chiamvimonvat N, Trayanova N, Bers D and Chen‐Izu Y (2020) Mechano‐electric and mechano‐chemo‐transduction in cardiomyocytes, The Journal of Physiology, 10.1113/JP276494, 598:7, (1285-1305), Online publication date: 1-Apr-2020. Caruel M, Moireau P and Chapelle D (2019) Stochastic modeling of chemical–mechanical coupling in striated muscles, Biomechanics and Modeling in Mechanobiology, 10.1007/s10237-018-1102-z, 18:3, (563-587), Online publication date: 1-Jun-2019. Chava R, Assis F, Herzka D and Kolandaivelu A (2018) Segmented radial cardiac MRI during arrhythmia using retrospective electrocardiogram and respiratory gating, Magnetic Resonance in Medicine, 10.1002/mrm.27533, 81:3, (1726-1738), Online publication date: 1-Mar-2019. Rusu M, Hilse K, Schuh A, Martin L, Slabu I, Stoppe C and Liehn E (2019) Biomechanical assessment of remote and postinfarction scar remodeling following myocardial infarction, Scientific Reports, 10.1038/s41598-019-53351-7, 9:1, Online publication date: 1-Dec-2019. Reda S, Gollapudi S and Chandra M (2019) Developmental increase in β-MHC enhances sarcomere length–dependent activation in the myocardium, Journal of General Physiology, 10.1085/jgp.201812183, 151:5, (635-644), Online publication date: 6-May-2019. Baker H, Kiel A, Luebbe S, Simon B, Earl C, Regmi A, Roell W, Mather K, Tune J and Goodwill A (2019) Inhibition of sodium–glucose cotransporter-2 preserves cardiac function during regional myocardial ischemia independent of alterations in myocardial substrate utilization, Basic Research in Cardiology, 10.1007/s00395-019-0733-2, 114:3, Online publication date: 1-May-2019. Reda S and Chandra M (2019) Dilated cardiomyopathy mutation (R174W) in troponin T attenuates the length-mediated increase in cross-bridge recruitment and myofilament Ca 2+ sensitivity , American Journal of Physiology-Heart and Circulatory Physiology, 10.1152/ajpheart.00171.2019, 317:3, (H648-H657), Online publication date: 1-Sep-2019. Schneider C, Forsythe L, Somauroo J, George K and Oxborough D (2018) The impact of preload reduction with head-up tilt testing on longitudinal and transverse left ventricular mechanics: a study utilizing deformation volume analysis, Echo Research & Practice, 10.1530/ERP-17-0064, 5:1, (11-18), Online publication date: 1-Mar-2018. Reda S and Chandra M (2018) Cardiomyopathy mutation (F88L) in troponin T abolishes length dependency of myofilament Ca2+ sensitivity, Journal of General Physiology, 10.1085/jgp.201711974, 150:6, (809-819), Online publication date: 4-Jun-2018. Aitchison Smith D (2018) Cooperative Muscular Activation by Calcium The Sliding-Filament Theory of Muscle Contraction, 10.1007/978-3-030-03526-6_8, (347-373), . Shiels H (2017) Cardiomyocyte Morphology and Physiology The Cardiovascular System - Morphology, Control and Function, 10.1016/bs.fp.2017.04.001, (55-98), . Gollapudi S, Reda S and Chandra M (2017) Omecamtiv Mecarbil Abolishes Length-Mediated Increase in Guinea Pig Cardiac Myofiber Ca2+ Sensitivity, Biophysical Journal, 10.1016/j.bpj.2017.07.002, 113:4, (880-888), Online publication date: 1-Aug-2017. Boulay E, Pugsley M, Jacquemet V, Vinet A, Accardi M, Soloviev M, Troncy E, Doyle J, Pierson J and Authier S (2017) Cardiac contractility: Correction strategies applied to telemetry data from a HESI-sponsored consortium, Journal of Pharmacological and Toxicological Methods, 10.1016/j.vascn.2017.04.009, 87, (38-47), Online publication date: 1-Sep-2017. Engle S (2016) Predictive Cardiac Hypertrophy Biomarkers in Nonclinical Studies Drug Discovery Toxicology, 10.1002/9781119053248.ch24, (385-396) Winslow R, Walker M and Greenstein J (2015) Modeling calcium regulation of contraction, energetics, signaling, and transcription in the cardiac myocyte, WIREs Systems Biology and Medicine, 10.1002/wsbm.1322, 8:1, (37-67), Online publication date: 1-Jan-2016. Szema A, Dang S and Li J (2015) Emerging Novel Therapies for Heart Failure, Clinical Medicine Insights: Cardiology, 10.4137/CMC.S29735, 9s2, (CMC.S29735), Online publication date: 1-Jan-2015. Heyen J and Vargas H (2015) The Use of Nonhuman Primates in Cardiovascular Safety Assessment The Nonhuman Primate in Nonclinical Drug Development and Safety Assessment, 10.1016/B978-0-12-417144-2.00029-9, (551-578), . Wang K, Terrar D, Gavaghan D, Mu-u-min R, Kohl P and Bollensdorff C (2014) Living cardiac tissue slices: An organotypic pseudo two-dimensional model for cardiac biophysics research, Progress in Biophysics and Molecular Biology, 10.1016/j.pbiomolbio.2014.08.006, 115:2-3, (314-327), Online publication date: 1-Aug-2014. Inoue T, Kobirumaki-Shimozawa F, Kagemoto T, Fujii T, Terui T, Kusakari Y, Hongo K, Morimoto S, Ohtsuki I, Hashimoto K and Fukuda N (2013) Depressed Frank–Starling mechanism in the left ventricular muscle of the knock-in mouse model of dilated cardiomyopathy with troponin T deletion mutation ΔK210, Journal of Molecular and Cellular Cardiology, 10.1016/j.yjmcc.2013.07.001, 63, (69-78), Online publication date: 1-Oct-2013. (2013) Further Reading Back to Basics in Physiology, 10.1016/B978-0-12-407168-1.00016-2, (151-152), . Gollapudi S, Mamidi R, Mallampalli S and Chandra M (2012) The N-Terminal Extension of Cardiac Troponin T Stabilizes the Blocked State of Cardiac Thin Filament, Biophysical Journal, 10.1016/j.bpj.2012.07.035, 103:5, (940-948), Online publication date: 1-Sep-2012. Clark K, Lesage-Horton H, Zhao C, Beckerle M and Swank D (2011) Deletion of Drosophila muscle LIM protein decreases flight muscle stiffness and power generation , American Journal of Physiology-Cell Physiology, 10.1152/ajpcell.00206.2010, 301:2, (C373-C382), Online publication date: 1-Aug-2011. Genin G, Abney T, Wakatsuki T and Elson E (2011) Cell-Cell Interactions and the Mechanics of Cells and Tissues Observed in Bioartificial Tissue Constructs Mechanobiology of Cell-Cell and Cell-Matrix Interactions, 10.1007/978-1-4419-8083-0_5, (75-103), . Eldred C, Simeonov D, Koppes R, Yang C, Corr D and Swank D (2010) The Mechanical Properties of Drosophila Jump Muscle Expressing Wild-Type and Embryonic Myosin Isoforms, Biophysical Journal, 10.1016/j.bpj.2009.11.051, 98:7, (1218-1226), Online publication date: 1-Apr-2010. de Tombe P, Mateja R, Tachampa K, Mou Y, Farman G and Irving T (2010) Myofilament length dependent activation, Journal of Molecular and Cellular Cardiology, 10.1016/j.yjmcc.2009.12.017, 48:5, (851-858), Online publication date: 1-May-2010. Terui T, Shimamoto Y, Yamane M, Kobirumaki F, Ohtsuki I, Ishiwata S, Kurihara S and Fukuda N (2010) Regulatory mechanism of length-dependent activation in skinned porcine ventricular muscle: role of thin filament cooperative activation in the Frank-Starling relation, Journal of General Physiology, 10.1085/jgp.201010502, 136:4, (469-482), Online publication date: 1-Oct-2010. Sun L and Schwarzenberger J (2010) Cardiac Physiology Miller's Anesthesia, 10.1016/B978-0-443-06959-8.00016-9, (393-410), . Wu X, Sun Z, Foskett A, Trzeciakowski J, Meininger G and Muthuchamy M (2010) Cardiomyocyte contractile status is associated with differences in fibronectin and integrin interactions, American Journal of Physiology-Heart and Circulatory Physiology, 10.1152/ajpheart.01156.2009, 298:6, (H2071-H2081), Online publication date: 1-Jun-2010. Smith G (2010) Frank–Starling law and mass action calcium activation of the myofibril ATPase; Comment on "de Tombe PP, Mateja RD, Tachampa K, Mou YA, Farman GP, Irving TC. Myofilament length dependent activation. J Mol Cell Cardiol 2010; 48: 851–8", Journal of Molecular and Cellular Cardiology, 10.1016/j.yjmcc.2010.07.003, 49:4, (707-708), Online publication date: 1-Oct-2010. Sela G and Landesberg A (2009) The external work–pressure time integral relationships and the afterload dependence of Frank–Starling mechanism, Journal of Molecular and Cellular Cardiology, 10.1016/j.yjmcc.2009.05.007, 47:4, (544-551), Online publication date: 1-Oct-2009. Boulpaep E (2009) THE HEART AS A PUMP Medical Physiology, 10.1016/B978-1-4160-3115-4.50025-1, (529-553), . Nagappan S, Rathinam A, Johnson K and Woo C Integration of Tension Development Model with the Fiber-Fluid Model of the Heart 4th Kuala Lumpur International Conference on Biomedical Engineering 2008, 10.1007/978-3-540-69139-6_13, (31-35) Ait mou Y, le Guennec J, Mosca E, de Tombe P and Cazorla O (2008) Differential contribution of cardiac sarcomeric proteins in the myofibrillar force response to stretch, Pflügers Archiv - European Journal of Physiology, 10.1007/s00424-008-0501-x, 457:1, (25-36), Online publication date: 1-Oct-2008. Pearson J, Shirai M, Tsuchimochi H, Schwenke D, Ishida T, Kangawa K, Suga H and Yagi N (2007) Effects of Sustained Length-Dependent Activation on In Situ Cross-Bridge Dynamics in Rat Hearts, Biophysical Journal, 10.1529/biophysj.107.111740, 93:12, (4319-4329), Online publication date: 1-Dec-2007. Makita N and Tsutsui H (2007) Genetic Polymorphisms and Arrhythmia Susceptibility, Circulation Journal, 10.1253/circj.71.A54, 71:SupplementA, (A54-A60), . Frazier S, Stone K, Moser D, Schlanger R, Carle C, Pender L, Widener J and Brom H (2006) Hemodynamic Changes During Discontinuation of Mechanical Ventilation in Medical Intensive Care Unit Patients, American Journal of Critical Care, 10.4037/ajcc2006.15.6.580, 15:6, (580-593), Online publication date: 1-Nov-2006. Niederer S, Hunter P and Smith N (2006) A Quantitative Analysis of Cardiac Myocyte Relaxation: A Simulation Study, Biophysical Journal, 10.1529/biophysj.105.069534, 90:5, (1697-1722), Online publication date: 1-Mar-2006. Stelzer J and Moss R (2006) Contributions of Stretch Activation to Length-dependent Contraction in Murine Myocardium, Journal of General Physiology, 10.1085/jgp.200609634, 128:4, (461-471), Online publication date: 1-Oct-2006. Asnes C, Marquez J, Elson E and Wakatsuki T (2006) Reconstitution of the Frank-Starling Mechanism in Engineered Heart Tissues, Biophysical Journal, 10.1529/biophysj.105.065961, 91:5, (1800-1810), Online publication date: 1-Sep-2006. Nyhan D and Blanck T (2006) Cardiac physiology Foundations of Anesthesia, 10.1016/B978-0-323-03707-5.50045-0, (473-484), . Schneider N, Shimayoshi T, Amano A and Matsuda T (2006) Mechanism of the Frank–Starling law—A simulation study with a novel cardiac muscle contraction model that includes titin and troponin I, Journal of Molecular and Cellular Cardiology, 10.1016/j.yjmcc.2006.06.003, 41:3, (522-536), Online publication date: 1-Sep-2006. Cazorla O, Szilagyi S, Le Guennec J, Vassort G and Lacampagne A (2004) Transmural stretch‐dependent regulation of contractile properties in rat heart and its alteration after myocardial infarction, The FASEB Journal, 10.1096/fj.04-2066fje, 19:1, (88-90), Online publication date: 1-Jan-2005. Fukuda N, Wu Y, Farman G, Irving T and Granzier H (2004) Titin-based modulation of active tension and interfilament lattice spacing in skinned rat cardiac muscle, Pfl�gers Archiv - European Journal of Physiology, 10.1007/s00424-004-1354-6, 449:5, (449-457), Online publication date: 1-Feb-2005. Mohler P, Rivolta I, Napolitano C, LeMaillet G, Lambert S, Priori S and Bennett V (2004) Na v 1.5 E1053K mutation causing Brugada syndrome blocks binding to ankyrin-G and expression of Na v 1.5 on the surface of cardiomyocytes , Proceedings of the National Academy of Sciences, 10.1073/pnas.0403711101, 101:50, (17533-17538), Online publication date: 14-Dec-2004. Martyn D, Adhikari B, Regnier M, Gu J, Xu S and Yu L (2004) Response of Equatorial X-Ray Reflections and Stiffness to Altered Sarcomere Length and Myofilament Lattice Spacing in Relaxed Skinned Cardiac Muscle, Biophysical Journal, 10.1016/S0006-3495(04)74175-2, 86:2, (1002-1011), Online publication date: 1-Feb-2004. Adhikari B, Regnier M, Rivera A, Kreutziger K and Martyn D (2004) Cardiac Length Dependence of Force and Force Redevelopment Kinetics with Altered Cross-Bridge Cycling, Biophysical Journal, 10.1529/biophysj.103.039131, 87:3, (1784-1794), Online publication date: 1-Sep-2004. Kaasik A, Joubert F, Ventura‐Clapier R and Veksler V (2004) A novel mechanism of regulation of cardiac contractility by mitochondrial functional state, The FASEB Journal, 10.1096/fj.04-1508com, 18:11, (1219-1227), Online publication date: 1-Aug-2004. Calaghan S, Belus A and White E (2003) Do stretch-induced changes in intracellular calcium modify the electrical activity of cardiac muscle?, Progress in Biophysics and Molecular Biology, 10.1016/S0079-6107(03)00007-5, 82:1-3, (81-95), Online publication date: 1-May-2003. Popović Z, Mowrey K, Zhang Y, Zhuang S, Tabata T, Wallick D, Grimm R, Thomas J and Mazgalev T (2002) Slow rate during AF improves ventricular performance by reducing sensitivity to cycle length irregularity, American Journal of Physiology-Heart and Circulatory Physiology, 10.1152/ajpheart.00571.2002, 283:6, (H2706-H2713), Online publication date: 1-Dec-2002. Malingen S, Asencio A, Cass J, Ma W, Irving T and Daniel T (2020) In vivo x-ray diffraction and simultaneous EMG reveal the time course of myofilament lattice dilation and filament stretch , Journal of Experimental Biology, 10.1242/jeb.224188 Uesugi K, Shima F, Fukumoto K, Hiura A, Tsukamoto Y, Miyagawa S, Sawa Y, Akagi T, Akashi M and Morishima K (2019) Micro Vacuum Chuck and Tensile Test System for Bio-Mechanical Evaluation of 3D Tissue Constructed of Human Induced Pluripotent Stem Cell-Derived Cardiomyocytes (hiPS-CM), Micromachines, 10.3390/mi10070487, 10:7, (487) Pirozzi I, Kight A, Shad R, Han A, Dual S, Fong R, Jia A, Hiesinger W, Yock P and Cutkosky M (2022) RVEX: Right Ventricular External Device for Biomimetic Support and Monitoring of the Right Heart, Advanced Materials Technologies, 10.1002/admt.202101472, (2101472) Fajardo G, Coronado M, Matthews M and Bernstein D (2022) Mitochondrial Quality Control in the Heart: The Balance between Physiological and Pathological Stress, Biomedicines, 10.3390/biomedicines10061375, 10:6, (1375) Sasaki D, Matsuura K, Seta H, Haraguchi Y, Okano T, Shimizu T and Aalto-Setala K (2018) Contractile force measurement of human induced pluripotent stem cell-derived cardiac cell sheet-tissue, PLOS ONE, 10.1371/journal.pone.0198026, 13:5, (e0198026) Li J, Hua Y, Miyagawa S, Zhang J, Li L, Liu L and Sawa Y (2020) hiPSC-Derived Cardiac Tissue for Disease Modeling and Drug Discovery, International Journal of Molecular Sciences, 10.3390/ijms21238893, 21:23, (8893) Lazarus A, Gao H, Luo X and Husmeier D (2022) Improving cardio‐mechanic inference by combining in vivo strain data with ex vivo volume–pressure data, Journal of the Royal Statistical Society: Series C (Applied Statistics), 10.1111/rssc.12560 January 11, 2002Vol 90, Issue 1 Advertisement Article InformationMetrics https://doi.org/10.1161/res.90.1.11PMID: 11786511 Originally publishedApril 3, 2018 KeywordsmyocardiumCa2+ sensitivityFrank-StarlingrelationshipPDF download Advertisement
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