Impact of myocyte strain on cardiac myofilament activation

Pflugers Archiv European Journal of Physiology

Volumn 462, Issue 1, 2011, Pages 3-14

  Campbell, Kenneth S ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

Muscle; Muscle mechanics; Muscle stretch; Myocardial contractility; Myofilament; Myosin; Ventricle; Ventricular myocyte

Indexed keywords

CONNECTIN; MYOSIN;

BLOOD VOLUME; CALCIUM CELL LEVEL; HEART LEFT VENTRICLE MUSCLE; HEART MUSCLE BLOOD FLOW; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART MUSCLE TENSION; HEART RIGHT VENTRICLE; HUMAN; MOLECULAR MECHANICS; MUSCLE DEVELOPMENT; MUSCLE FIBRIL; MUSCLE STRETCHING; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; SARCOMERE; STARLING LAW; STRESS STRAIN RELATIONSHIP;

ANIMALS; CALCIUM; MECHANOTRANSDUCTION, CELLULAR; MICROFILAMENTS; MUSCLE PROTEINS; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PROTEIN KINASES; SARCOMERES; STRESS, MECHANICAL;

EID: 79958813862     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-011-0952-3     Document Type: Review

References (55)

1. DG Allen S Kurihara 1982 The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle J Physiol 327 79 94 7120151 1:CAS:528:DyaL38XktlKlsLk%3D (Pubitemid 12086440)
2. JS Allingham R Smith I Rayment 2005 The structural basis of blebbistatin inhibition and specificity for myosin II Nat Struct Mol Biol 12 378 379 15750603 10.1038/nsmb908 1:CAS:528:DC%2BD2MXivFWjtLo%3D (Pubitemid 43093094)
3. MA Bagni G Cecchi B Colombini F Colomo 2002 A non-cross-bridge stiffness in activated frog muscle fibers Biophys J 82 3118 3127 12023235 10.1016/S0006-3495(02)75653-1 1:CAS:528:DC%2BD38Xkt1Srsro%3D (Pubitemid 34547655)
4. K Campbell 1997 Rate constant of muscle force redevelopment reflects cooperative activation as well as cross-bridge kinetics Biophys J 72 254 262 8994610 10.1016/S0006-3495(97)78664-8 1:CAS:528:DyaK2sXmtFOiuw%3D%3D (Pubitemid 27043435)
5. KS Campbell 2006 Filament compliance effects can explain tension overshoots during force development Biophys J 91 4102 4109 16950846 10.1529/biophysj.106.087312 1:CAS:528:DC%2BD28Xht1KhtbfL (Pubitemid 44887270)
6. KS Campbell 2009 Interactions between connected half-sarcomeres produce emergent behavior in a mathematical model of muscle PLOS Computational Biology 5 e1000560 10.1371/journal.pcbi.1000560 19911050 10.1371/journal.pcbi.1000560
7. KS Campbell 2010 Short-range mechanical properties of skeletal and cardiac muscles Adv Exp Med Biol 682 223 246 20824529 10.1007/978-1-4419-6366-6- 13
8. KS Campbell RL Moss 2000 A thixotropic effect in contracting rabbit psoas muscle: prior movement reduces the initial tension response to stretch J Physiol 525 2 531 548 10835052 10.1111/j.1469-7793.2000.00531.x 1:CAS:528:DC%2BD3cXktl2ktrc%3D (Pubitemid 30398379)
9. SG Campbell FV Lionetti KS Campbell AD McCulloch 2010 Coupling of adjacent tropomyosins enhances cross-bridge-mediated cooperative activation in a Markov model of the cardiac thin filament Biophys J 98 2254 2264 20483334 10.1016/j.bpj.2010.02.010 1:CAS:528:DC%2BC3cXosFCisbg%3D
10. O Cazorla G Vassort D Garnier J-Y Le Guennec 1999 Length modulation of active force in rat cardiac myocytes: is titin the sensor? J Mol Cell Cardiol 31 1215 1227 10371696 10.1006/jmcc.1999.0954 1:CAS:528:DyaK1MXjslOqtbY%3D (Pubitemid 29276619)
11. O Cazorla Y Wu TC Irving H Granzier 2001 Titin-based modulation of calcium sensitivity of active tension in mouse skinned cardiac myocytes Circ Res 88 1028 1035 11375272 10.1161/hh1001.090876 1:CAS:528:DC%2BD3MXktFOls7w%3D (Pubitemid 34137115)
12. C Chapman E Wasserman 1960 On the dynamics of cardiac muscle Am Heart J 58 272 317 Originally published, in German, in: Zeitschrift für Biologie. (1895) 32:370-447
13. TL Daniel AC Trimble PB Chase 1998 Compliant realignment of binding sites in muscle: transient behavior and mechanical tuning Biophys J 74 1611 1621 9545027 10.1016/S0006-3495(98)77875-0 1:CAS:528:DyaK1cXislSksL4%3D (Pubitemid 28157903)
14. PP de Tombe RD Mateja K Tachampa YA Mou GP Farman TC Irving 2010 Myofilament length dependent activation J Mol Cell Cardiol 48 851 858 20053351 10.1016/j.yjmcc.2009.12.017
15. DP Dobesh JP Konhilas PP de Tombe 2002 Cooperative activation in cardiac muscle: impact of sarcomere length Am J Physiol Heart Circ Physiol 282 H1055 H1062 11834504 1:CAS:528:DC%2BD38Xit1Ghu7Y%3D
16. A Fabiato F Fabiato 1975 Dependence of the contractile activation of skinned cardiac cells on the sarcomere length Nature 256 54 56 1134580 10.1038/256054a0 1:STN:280:DyaE2M7nsFaqsg%3D%3D
17. GP Farman EJ Allen KQ Schoenfelt PH Backx PP de Tombe 2010 The role of thin filament cooperativity in cardiac length-dependent calcium activation Biophys J 99 2978 2986 21044595 10.1016/j.bpj.2010.09.003 1:CAS:528: DC%2BC3cXhtlKkur%2FL
18. 2+ activation of rat ventricular myocytes Circ Res 83 6 602 607 9742055 1:CAS:528:DyaK1cXmt1Knt7o%3D (Pubitemid 28427743)
19. LE Ford AF Huxley RM Simmons 1981 The relation between stiffness and filament overlap in stimulated frog muscle fibres J Physiol 311 219 249 6973625 1:STN:280:DyaL3M3ms1yqsw%3D%3D (Pubitemid 11166918)
20. F Fuchs SH Smith 2001 Calcium, cross-bridges, and the Frank-Starling relationship News Physiol Sci 16 5 10 11390938 1:CAS:528:DC%2BD3MXjsV2ntb8%3D (Pubitemid 33574449)
21. H Fujita D Labeit B Gerull S Labeit HL Granzier 2004 Titin isoform-dependent effect of calcium on passive myocardial tension Am J Physiol, Heart Circ Physiol 287 H2528 H2534 10.1152/ajpheart.00553.2004 1:CAS:528:DC%2BD2cXhtVOmurjL (Pubitemid 39557121)
22. N Fukuda D Sasaki S Ishiwata S Kurihara 2001 Length dependence of tension generation in rat skinned cardiac muscle: role of titin in the Frank-Starling mechanism of the heart Circulation 104 1639 1645 11581142 10.1161/hc3901.095898 1:CAS:528:DC%2BD3MXotVeht7s%3D (Pubitemid 32947527)
23. AM Gordon E Homsher M Regnier 2000 Regulation of contraction in striated muscle Physiol Rev 80 853 924 10747208 1:CAS:528:DC%2BD3cXisFSgsr8%3D (Pubitemid 30164950)
24. HL Granzier S Labeit 2004 The giant protein titin: a major player in myocardial mechanics, signaling, and disease Circ Res 94 284 295 14976139 10.1161/01.RES.0000117769.88862.F8 1:CAS:528:DC%2BD2cXhtFWksrk%3D (Pubitemid 38240719)
25. M Helmes K Trombitas H Granzier 1996 Titin develops restoring force in rat cardiac myocytes Circ Res 79 619 626 8781495 1:CAS:528:DyaK28XlsVOns7s%3D (Pubitemid 26276922)
26. M Helmes CC Lim R Liao A Bharti L Cui DB Sawyer 2003 Titin determines the Frank-Starling relation in early diastole J Gen Physiol 121 97 110 12566538 10.1085/jgp.20028652 1:CAS:528:DC%2BD3sXhs1yntL4%3D (Pubitemid 36255340)
27. TJ Herron E Rostkova G Kunst R Chaturvedi M Gautel JC Kentish 2006 Activation of myocardial contraction by the N-terminal domains of myosin binding protein-C Circ Res 98 1290 1298 16614305 10.1161/01.RES.0000222059.54917.ef 1:CAS:528:DC%2BD28XkslKrtbs%3D (Pubitemid 43948084)
28. MG Hibberd BR Jewell 1982 Calcium- and length-dependent force production in rat ventricular muscle J Physiol 329 527 540 7143258 1:CAS:528: DyaL38XkslSisrk%3D (Pubitemid 12057930)
29. HE Huxley A Stewart H Sosa T Irving 1994 X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle Biophys J 67 2411 2421 7696481 10.1016/S0006-3495(94)80728-3 1:CAS:528: DyaK2MXisVajurc%3D (Pubitemid 24369665)
30. AM Katz 2002 Ernest Henry Starling, his predecessors, and the "Law of the Heart" Circulation 106 2986 2992 12460884 10.1161/01.CIR.0000040594. 96123.55
31. JC Kentish HE ter Keurs L Ricciardi JJ Bucx MI Noble 1986 Comparison between the sarcomere length-force relations of intact and skinned trabeculae from rat right ventricle. Influence of calcium concentrations on these relations Circ Res 58 755 768 3719928 1:CAS:528:DyaL28Xkt1ahu7o%3D (Pubitemid 16094206)
32. JP Konhilas TC Irving PP De Tombe 2002 Myofilament calcium sensitivity in skinned rat cardiac trabecule. Role of interfilament spacing Circ Res 90 59 65 11786519 10.1161/hh0102.102269 1:CAS:528:DC%2BD38XotlSjsQ%3D%3D (Pubitemid 34074609)
33. D Labeit K Watanabe C Witt H Fujita Y Wu S Lahmers T Funck S Labeit H Granzier 2003 Calcium-dependent molecular spring elements in the giant protein titin Proc Natl Acad Sci USA 100 13716 13721 14593205 10.1073/pnas.2235652100 1:CAS:528:DC%2BD3sXptFOiurs%3D (Pubitemid 37444805)
34. JY Le Guennec N Peineau JA Argibay KG Mongo D Garnier 1990 A new method of attachment of isolated mammalian ventricular myocytes for tension recording: length dependence of passive and active tension J Mol Cell Cardiol 22 1083 1093 2095433 10.1016/0022-2828(90)90072-A (Pubitemid 20378821)
35. EJ Lee J Peng M Radke M Gotthardt HL Granzier 2010 Calcium sensitivity and the Frank-Starling mechanism of the heart are increased in titin N2B region-deficient mice J Mol Cell Cardiol 49 449 458 20507834 10.1016/j.yjmcc.2010.05.006 1:CAS:528:DC%2BC3cXpvV2gurw%3D
36. TR Leonard W Herzog 2010 Regulation of muscle force in the absence of actin-myosin-based cross-bridge interaction Am J Physiol Cell Physiol 299 C14 C20 20357181 10.1152/ajpcell.00049.2010 1:CAS:528:DC%2BC3cXpslSgs78%3D
37. I Matsubara BM Millman 1974 X-ray diffraction patterns from mammalian heart muscle J Mol Biol 82 527 536 4817795 10.1016/0022-2836(74)90246-0 1:STN:280:DyaE2c7islWgsg%3D%3D
38. KS McDonald RL Moss 1995 Osmotic compression of single cardiac myocytes eliminates the reduction in Ca2+ sensitivity of tension at short sarcomere length Circ Res 77 199 205 7788878 1:CAS:528:DyaK2MXmsFersbc%3D
39. DL Morgan 1990 New insights into the behavior of muscle during active lengthening Biophys J 57 2 209 221 2317547 10.1016/S0006-3495(90)82524-8 1:STN:280:DyaK3c7pvFShsQ%3D%3D (Pubitemid 20058256)
40. RL Moss DP Fitzsimons 2002 Frank-Starling relationship: long on importance, short on mechanism Circ Res 90 11 13 11786511 10.1161/hh0102.102977 1:CAS:528:DC%2BD38XotFWiug%3D%3D (Pubitemid 34074601)
41. C Muhle-Goll M Habeck O Cazorla M Nilges S Labeit H Granzier 2001 Structural and functional studies of titin's fn3 modules reveal conserved surface patterns and binding to myosin S1-a possible role in the Frank-Starling mechanism of the heart J Mol Biol 313 431 447 11800567 10.1006/jmbi.2001.5017 1:CAS:528:DC%2BD3MXotVyntrc%3D (Pubitemid 33587198)
42. WW Parmley L Chuck 1973 Length-dependent changes in myocardial contractile state Am J Physiol 224 1195 1199 4700639 1:STN:280: DyaE3s7mslWjsQ%3D%3D
43. JJ Rice F Wang DM Bers PP de Tombe 2008 Approximate model of cooperative activation and crossbridge cycling in cardiac muscle using ordinary differential equations Biophys J 95 2368 2390 18234826 10.1529/biophysj.107.119487 1:CAS:528:DC%2BD1cXhtVGqsrzI
44. GA Smith 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: 851-858" J Mol Cell Cardiol 49 707 708 20624395 10.1016/j.yjmcc.2010.07.003 1:CAS:528:DC%2BC3cXhtVyrurjL author reply 709
45. DA Smith MA Geeves J Sleep SM Mijailovich 2008 Towards a unified theory of muscle contraction. I: foundations Ann Biomed Eng 36 1624 1640 18642081 10.1007/s10439-008-9536-6 1:STN:280:DC%2BD1crpt1KntQ%3D%3D
46. Starling E (1918) The Linacre lecture on the law of the heart. Longmans, Green and Co, London
47. U Stoecker IA Telley E Stussi J Denoth 2009 A multisegmental cross-bridge kinetics model of the myofibril J Theor Biol 259 714 726 19348814 10.1016/j.jtbi.2009.03.032 1:CAS:528:DC%2BD1MXovF2qs78%3D
48. YB Sun F Lou M Irving 2009 Calcium- and myosin-dependent changes in troponin structure during activation of heart muscle J Physiol 587 155 163 19015190 10.1113/jphysiol.2008.164707 1:CAS:528:DC%2BD1MXhtVKlsL8%3D
49. DR Swartz RL Moss 1992 Influence of a strong-binding myosin analogue on calcium-sensitive mechanical properties of skinned skeletal muscle fibers J Biol Chem 267 20497 20506 1400367 1:CAS:528:DyaK38XlsVOqu7c%3D
50. K Tachampa H Wang GP Farman PP de Tombe 2007 Cardiac troponin I threonine 144: role in myofilament length dependent activation Circ Res 101 1081 1083 17975107 10.1161/CIRCRESAHA.107.165258 1:CAS:528:DC%2BD2sXhtlahurjK (Pubitemid 350146433)
51. BCW Tanner AH Danser M Regnier 2007 Sarcomere lattice geometry influences cooperative myosin binding in muscle PLOS Computational Biology 3 e115 17630823 10.1371/journal.pcbi.0030115 (Pubitemid 47196164)
52. IA Telley J Denoth E Stussi G Pfitzer R Stehle 2006 Half-sarcomere dynamics in myofibrils during activation and relaxation studied by tracking fluorescent markers Biophys J 90 514 530 16239326 10.1529/biophysj.105.070334 1:CAS:528:DC%2BD28XktlKksw%3D%3D
53. HEDJ ter Keurs WH Rijnsburger R van Heuningen MJ Nagelsmit 1980 Tension development and sarcomere length in rat cardiac trabeculae Circ Res 46 703 714 7363419
54. K Wakabayashi Y Sugimoto H Tanaka Y Ueno Y Takezawa Y Amemiya 1994 X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction Biophys J 67 2422 2435 7779179 10.1016/S0006-3495(94)80729-5 1:CAS:528:DyaK2MXisVaju74%3D (Pubitemid 24369666)
55. CD Williams M Regnier TL Daniel 2010 Axial and radial forces of cross-bridges depend on lattice spacing PLoS Comput Biol 6 e1001018 21152002 10.1371/journal.pcbi.1001018