دورية أكاديمية
Biomechanical evaluation of flash-frozen and cryo-sectioned papillary muscle samples by using sinusoidal analysis: cross-bridge kinetics and the effect of partial Ca 2+ activation.
| العنوان: | Biomechanical evaluation of flash-frozen and cryo-sectioned papillary muscle samples by using sinusoidal analysis: cross-bridge kinetics and the effect of partial Ca 2+ activation. |
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| المؤلفون: | Xi J; School of Nursing, and Medical Skill Experiment Teaching Center, Suzhou Medical College, Soochow University, Suzhou, 215006, China.; Department of Anatomy and Cell Biology, College of Medicine, University of Iowa, Iowa City, IA, 52242, USA., Feng HZ; Department of Physiology and Biophysics, University of Illinois at Chicago, 835 S Wolcott Ave, Chicago, IL, 60612, USA., Jin JP; Department of Physiology and Biophysics, University of Illinois at Chicago, 835 S Wolcott Ave, Chicago, IL, 60612, USA., Yuan J; The Collaborative Innovation Center, Jining Medical University, Jining, 272067, China., Kawai M; Department of Anatomy and Cell Biology, College of Medicine, University of Iowa, Iowa City, IA, 52242, USA. masataka-kawai@uiowa.edu. |
| المصدر: | Journal of muscle research and cell motility [J Muscle Res Cell Motil] 2024 Apr 16. Date of Electronic Publication: 2024 Apr 16. |
| Publication Model: | Ahead of Print |
| نوع المنشور: | Journal Article |
| اللغة: | English |
| بيانات الدورية: | Publisher: Springer Netherlands Country of Publication: Netherlands NLM ID: 8006298 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1573-2657 (Electronic) Linking ISSN: 01424319 NLM ISO Abbreviation: J Muscle Res Cell Motil Subsets: MEDLINE |
| أسماء مطبوعة: | Publication: Dordrecht : Springer Netherlands Original Publication: [London] Chapman and Hall. |
| مستخلص: | We examined the integrity of flash-frozen and cryo-sectioned cardiac muscle preparations (introduced by Feng and Jin, 2020) by assessing tension transients in response to sinusoidal length changes at varying frequencies (1-100 Hz) at 25 °C. Using 70-μm-thick sections, we isolated fiber preparations to study cross-bridge (CB) kinetics: preparations were activated by saturating Ca 2+ as well as varying concentrations of ATP and phosphate (Pi). Our results showed that, compared to ordinary skinned fibers, in-series stiffness decreased to 1/2, which resulted in a decrease of isometric tension to 62%, but CB kinetics and Ca 2+ sensitivity were little affected. The pCa study demonstrated that the rate constant of the force generation step (2πb) is proportionate to [Ca 2+ ] at < 5 μM, suggesting that the activation mechanism can be described by a simple second order reaction. We also found that tension, stiffness, and magnitude parameters are related to [Ca 2+ ] by the Hill equation, with a cooperativity coefficient of 4-5, which is consistent with the fact that Ca 2+ activation mechanisms involve cooperative multimolecular interactions. Our results support the long-held hypothesis that Process C (Phase 2) represents the CB detachment step, and Process B (Phase 3) represents the force generation step. Moreover, we discovered that constant H may represent the work-performing step in cardiac preparations. Our experiments demonstrate excellent CB kinetics with two well-defined exponentials that can be more distinguished than those found using ordinary skinned fibers. Flash-frozen and cryo-sectioned preparations are especially suitable for multi-institutional collaborations nationally and internationally because of their ease of transportation. (© 2024. The Author(s), under exclusive licence to Springer Nature Switzerland AG.) |
| التعليقات: | Update of: Res Sq. 2023 Nov 01;:. (PMID: 37961283) |
| References: | Abbott RH, Steiger GJ (1977) Temperature and amplitude dependence of tension transients in glycerinated skeletal and insect fibrillar muscle. J Physiol 266:13–42. (PMID: 856995128355110.1113/jphysiol.1977.sp011754) Bai F, Caster HM, Rubenstein PA, Dawson JF, Kawai M (2014) Using baculovirus/insect cell expressed recombinant actin to study the molecular pathogenesis of HCM caused by actin mutation A331P. J Mol Cell Cardiol 74C:64–75. (PMID: 10.1016/j.yjmcc.2014.04.014) Bartoo ML, Popov VI, Fearn LA, Pollack GH (1993) Active tension generation in isolated skeletal myofibrils. J Muscle Res Cell Motil 14:498–510. (PMID: 830084510.1007/BF00297212) Colomo F, Piroddi N, Poggesi C, te Kronnie G, Tesi C (1997) Active and passive forces of isolated myofibrils from cardiac and fast skeletal muscle of the frog. J Physiol 500(Pt 2):535–548. (PMID: 9147336115940210.1113/jphysiol.1997.sp022039) Dantzig J, Goldman Y, Millar NC, Lacktis J, Homsher E (1992) Reversal of the cross-bridge force-generating transition by the photogeneration of phosphate in rabbit psoas muscle fibers. J Physiol 451:247–278. (PMID: 1403812117616010.1113/jphysiol.1992.sp019163) Feng HZ, Jin JP (2020) High efficiency preparation of skinned mouse cardiac muscle strips from cryosections for contractility studies. Exp Physiol 105:1869–1881. (PMID: 3285788810.1113/EP088521) Ford LE, Huxley AF, Simmons RM (1977) Tension responses to sudden length change in stimulated frog muscle fibres near slack length. J Physiol 269:441–515. (PMID: 302333128372210.1113/jphysiol.1977.sp011911) Fortune NS, Geeves MA, Ranatunga KW (1991) Tension responses to rapid pressure release in glycerinated rabbit muscle fibers. Proc Natl Acad Sci USA 88:7323–7327. (PMID: 18711405228710.1073/pnas.88.16.7323) Gordon AM, Huxley AF, Julian FJ (1966) The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol 184:170–192. (PMID: 5921536135755310.1113/jphysiol.1966.sp007909) Gutfreund H (1995) Kinetics for life sciences: receptors, transmitters and chatalysts. Cambridge University Press. (PMID: 10.1017/CBO9780511626203) Harris DE, Warshaw DM (1993) Smooth and skeletal muscle actin are mechanically indistinguishable in the in vitro motility assay. Circ Res 72:219–224. (PMID: 841784410.1161/01.RES.72.1.219) Heinl P, Kuhn HJ, Ruegg JC (1974) Tension responses to quick length changes of glycerinated skeletal muscle fibres from the frog and tortoise. J Physiol 237:243–258. (PMID: 4545181135088210.1113/jphysiol.1974.sp010480) Hellam DC, Podolsky RJ (1969) Force measurements in skinned muscle fibres. J Physiol 200:807–819. (PMID: 5765859135052810.1113/jphysiol.1969.sp008723) Hibberd MG, Dantzig JA, Trentham DR, Goldman YE (1985) Phosphate release and force generation in skeletal muscle fibers. Science 228:1317–1319. (PMID: 315909010.1126/science.3159090) Hill AV (1910) The possible effects of the aggregation of the molecules of haemoglobin on its dissociation curves. J Physiol 40(Suppl):4–7. Hill AV (1938) The heat of shortening and the dynamic constants of muscle. Proc Roy Soc (b) 126:136–195. Hill AV (1953) The mechanics of active muscle. Proc R Soc Lond B Biol Sci 141:104–117. (PMID: 1304727610.1098/rspb.1953.0027) Huxley AF (1974) Muscular contraction. J Physiol 243:1–43. (PMID: 4449057133068710.1113/jphysiol.1974.sp010740) Huxley AF, Simmons RM (1971) Proposed mechanism of force generation in striated muscle. Nature 233:533–538. (PMID: 493997710.1038/233533a0) Jalal N, Zidi M (2018) Effect of cryopreservation at -80°C on visco-hyperelastic properties of skeletal muscle tissue. J Mech Behav Biomed Mater 77:572–577. (PMID: 2909612210.1016/j.jmbbm.2017.10.006) Julian FJ (1969) Activation in a skeletal muscle contraction model with a modification for insect fibrillar muscle. Biophys J 9:547–570. (PMID: 5778185136753610.1016/S0006-3495(69)86403-9) Kawai M, Brandt PW (1980) Sinusoidal analysis: a high resolution method for correlating biochemical reactions with physiological processes in activated skeletal muscles of rabbit, frog and crayfish. J Muscle Res Cell Mot 1:279–303. (PMID: 10.1007/BF00711932) Kawai M, Halvorson H (1989) Role of MgATP and MgADP in the crossbridge kinetics in chemically skinned rabbit psoas fibers. Study of a fast exponential process C. Biophys J 55:595–603. (PMID: 2785822133054210.1016/S0006-3495(89)82857-7) Kawai M, Halvorson HR (1991) Two step mechanism of phosphate release and the mechanism of force generation in chemically skinned fibers of rabbit psoas. Biophys J 59:329–342. (PMID: 2009356128115010.1016/S0006-3495(91)82227-5) Kawai M, Zhao Y (1993) Cross-bridge scheme and force per cross-bridge state in skinned rabbit psoas muscle fibers. Biophys J 65:638–651. (PMID: 8218893122576610.1016/S0006-3495(93)81109-3) Kawai M, Brandt P, Orentlicher M (1977) Dependence of energy transduction in intact skeletal muscles on the time in tension. Biophys J 18:161–172. (PMID: 140712147328210.1016/S0006-3495(77)85605-1) Kawai M, Saeki Y, Zhao Y (1993) Cross-bridge scheme and the kinetic constants of elementary steps deduced from chemically skinned papillary and trabecular muscles of the ferret. Circ Res 73:35–50. (PMID: 850853310.1161/01.RES.73.1.35) Kawai M, Stehle R, Pfitzer G, Iorga B (2021) Phosphate has dual roles in cross-bridge kinetics in rabbit psoas single myofibrils. J Gen Physiol. https://doi.org/10.1085/jgp.202012755. (PMID: 10.1085/jgp.202012755335996807885270) Kushmerick MJ, Moerland TS, Wiseman RW (1992) Mammalian skeletal muscle fibers distinguished by contents of phosphocreatine, ATP, and Pi. Proc Natl Acad Sci USA 89:7521–7525. (PMID: 15021634974210.1073/pnas.89.16.7521) Lu X, Tobacman LS, Kawai M (2003) Effects of tropomyosin internal deletion Delta23Tm on isometric tension and the cross-bridge kinetics in bovine myocardium. J Physiol 553:457–471. (PMID: 14500764234355710.1113/jphysiol.2003.053694) Lu X, Bryant MK, Bryan KE, Rubenstein PA, Kawai M (2005) Role of the N-terminal negative charges of actin in force generation and cross-bridge kinetics in reconstituted bovine cardiac muscle fibres. J Physiol 564:65–82. (PMID: 15649975145603810.1113/jphysiol.2004.078055) Lu X, Tobacman LS, Kawai M (2006) Temperature-dependence of isometric tension and cross-bridge kinetics of cardiac muscle fibers reconstituted with a tropomyosin internal deletion mutant. Biophys J 91:4230–4240. (PMID: 16980359163565510.1529/biophysj.106.084608) Lu X, Heeley DH, Smillie LB, Kawai M (2010) The role of tropomyosin isoforms and phosphorylation in force generation in thin-filament reconstituted bovine cardiac muscle fibres. J Muscle Res Cell Motil 31:93–109. (PMID: 20559861308990010.1007/s10974-010-9213-x) Pinzauti F, Pertici I, Reconditi M, Narayanan T, Stienen GJM, Piazzesi G, Lombardi V, Linari M, Caremani M (2018) The force and stiffness of myosin motors in the isometric twitch of a cardiac trabecula and the effect of the extracellular calcium concentration. J Physiol 596:2581–2596. (PMID: 29714038602383410.1113/JP275579) Piroddi N, Belus A, Scellini B, Tesi C, Giunti G, Cerbai E, Mugelli A, Poggesi C (2007) Tension generation and relaxation in single myofibrils from human atrial and ventricular myocardium. Pflugers Arch 454:63–73. (PMID: 1712309810.1007/s00424-006-0181-3) Podolsky RJ (1960) Kinetics of muscular contraction: the approach to the steady state. Nature 188:666–668. (PMID: 1373649310.1038/188666a0) Pringle JW (1967) The contractile mechanism of insect fibrillar muscle. Prog Biophys Mol Biol 17:1–60. (PMID: 422612410.1016/0079-6107(67)90003-X) Rassier DE, Herzog W, Pollack GH (2003) Dynamics of individual sarcomeres during and after stretch in activated single myofibrils. Proc Biol Sci 270:1735–1740. (PMID: 12965002169142410.1098/rspb.2003.2418) Reuben JP, Brandt PW, Berman M, Grundfest H (1971) Regulation of tension in the skinned crayfish muscle fiber. I. Contraction and relaxation in the absence of Ca (pCa is greater than 9). J Gen Physiol 57:385–407. (PMID: 5549096220311210.1085/jgp.57.4.385) Ruegg JC, Tregear RT (1966) Mechanical factors affecting the ATPase activity of glycerol-extracted insect fibrillar flight muscle. Proc R Soc Lond B Biol Sci 165:497–512. (PMID: 438057310.1098/rspb.1966.0080) Shibata T, Hunter WC, Sagawa K (1987) Dynamic stiffness of barium-contractured cardiac muscles with different speeds of contraction. Circ Res 60:770–779. (PMID: 295471910.1161/01.RES.60.5.770) Stehle R, Kruger M, Pfitzer G (2002) Force kinetics and individual sarcomere dynamics in cardiac myofibrils after rapid ca(2+) changes. Biophys J 83:2152–2161. (PMID: 12324432130230310.1016/S0006-3495(02)73975-1) Sugi H, Gomi S (1984) Cinematographic studies on the A-band length changes during Ca-activated contraction in horseshoe crab muscle myofibrils. Adv Exp Med Biol 170:107–118. (PMID: 674169010.1007/978-1-4684-4703-3_10) Tesi C, Colomo F, Nencini S, Pirodi N, Poggesi C (2000) The effect of inorganic phosphate on force generation in single myofibrils from rabbit skeletal muscle. Biophy J 78:3081–3092. (PMID: 10.1016/S0006-3495(00)76845-7) Walker JW, Lu Z, Moss R (1992) Effects of Ca2+ on the kinetics of phosphate release in skeletal muscle. J Biol Chem 267:2459–2466. (PMID: 173394510.1016/S0021-9258(18)45901-7) Wang G, Kawai M (1997) Force generation and phosphate release steps in skinned rabbit soleus slow-twitch muscle fibers. Biophys J 73:878–894. (PMID: 9251805118098510.1016/S0006-3495(97)78121-9) Wang L, Kawai M (2013) A re-interpretation of the rate of tension redevelopment (kTR) in active muscle. J Muscle Res Cell Motil 34:407–415. (PMID: 24162314390947010.1007/s10974-013-9366-5) Wang L, Muthu P, Szczesna-Cordary D, Kawai M (2013a) Characterizations of myosin essential light chain’s N-terminal truncation mutant Delta43 in transgenic mouse papillary muscles by using tension transients in response to sinusoidal length alterations. J Muscle Res Cell Motil 34:93–105. (PMID: 2339707410.1007/s10974-013-9337-x) Wang L, Muthu P, Szczesna-Cordary D, Kawai M (2013b) Diversity and similarity of motor function and cross-bridge kinetics in papillary muscles of transgenic mice carrying myosin regulatory light chain mutations D166Vand R58Q. J Mol Cell Cardiol 62:153–163. (PMID: 2372723310.1016/j.yjmcc.2013.05.012) Wang L, Sadayappan S, Kawai M (2014) Cardiac myosin binding protein C phosphorylation affects cross-bridge cycle’s elementary steps in a site-specific manner. PLoS ONE 0113417:1–21. Wannenburg T, Heijne GH, Geerdink JH, Van-Den-Dool HW, Janssen PM, DeTombe PP (2000) Cross-bridge kinetics in rat myocardium: effect of sarcomere length and calcium activation. Am J Physiol 279:H779–H790. Webb M, del Jackson R, Stewart TJ, Dugan SP, Carter MS, Cremo CR, Baker JE (2013) The myosin duty ratio tunes the calcium sensitivity and cooperative activation of the thin filament. Biochemistry 52:6437–6444. (PMID: 2394775210.1021/bi400262h) White DC, Thorson J (1972) Phosphate starvation and the nonlinear dynamics of insect fibrillar flight muscle. J Gen Physiol 60:307–336. (PMID: 5055791222607210.1085/jgp.60.3.307) Woody MS, Winkelmann DA, Capitanio M, Ostap EM, Goldman YE (2019) Single molecule mechanics resolves the earliest events in force generation by cardiac myosin. Elife, 8. Xi J, Ye Y, Mokadem M, Yuan J, Kawai M (2022) The effect of gender and obesity in modulating cross-bridge function in cardiac muscle fibers. J Muscle Res Cell Motil 43:157–172. (PMID: 3599422110.1007/s10974-022-09627-z) Zhang J, Wang L, Kazmierczak K, Yun H, Szczesna-Cordary D, Kawai M (2021) Hypertrophic cardiomyopathy associated E22K mutation in myosin regulatory light chain decreases calcium-activated tension and stiffness and reduces myofilament Ca(2+) sensitivity. Febs J 288:4596–4613. (PMID: 33548158866816310.1111/febs.15753) Zhao Y, Kawai M (1996) Inotropic agent EMD 53998 weakens nucleotide and phosphate binding to cross bridges in porcine myocardium. Am J Physiol 271:H1394–H1406. (PMID: 8897933) |
| معلومات مُعتمدة: | 600791001 Research Start-up Fund of Jining Medical University; HL127691 Office of Extramural Research, National Institutes of Health; HL138007 National Institute for Health Care Management Foundation |
| فهرسة مساهمة: | Keywords: Ca2+; Cryo-sectioned papillary muscle; Flash-frozen muscle preparation; Phosphate. ATP; Stiffness; Tension |
| تواريخ الأحداث: | Date Created: 20240416 Latest Revision: 20240506 |
| رمز التحديث: | 20240506 |
| DOI: | 10.1007/s10974-024-09667-7 |
| PMID: | 38625452 |
| قاعدة البيانات: | MEDLINE |
Find this article in full text from Springer Verlag. 
Full Text Finder | تدمد: | 1573-2657 |
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| DOI: | 10.1007/s10974-024-09667-7 |