Mouse intact cardiac myocyte mechanics: Cross-bridge and titin-based stress in unactivated cells

Journal of General Physiology

Volumn 137, Issue 1, 2011, Pages 81-91

  King, Nicholas M P ^a,b   Methawasin, Methajit ^a   Nedrud, Joshua ^a   Harrell, Nicholas ^a   Chung, Charles S ^a   Helmes, Michiel ^c   Granzier, Henk ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2,3 BUTANEDIONE; BLEBBISTATIN; CALCIUM; CARBON; CARBON FIBER; CONNECTIN; DIACETYL OXIME; DRUG DERIVATIVE; FUSED HETEROCYCLIC RINGS; MUSCLE PROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE; PROTEIN KINASE;

ANIMAL; ARTICLE; BLOOD PRESSURE; C57BL MOUSE; DRUG ANTAGONISM; DRUG EFFECT; HEART; HEART CONTRACTION; HEART MUSCLE CELL; MALE; MECHANICAL STRESS; METABOLISM; MICROFILAMENT; MOUSE; PHYSIOLOGY; SARCOMERE;

ACTOMYOSIN; ANIMALS; BLOOD PRESSURE; CALCIUM; CARBON; DIACETYL; HEART; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; MALE; MICE; MICE, INBRED C57BL; MICROFILAMENTS; MUSCLE PROTEINS; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PROTEIN KINASES; SARCOMERES; STRESS, MECHANICAL;

EID: 78650890427     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201010499     Document Type: Article

References (56)

1. Adhikari, B.B., M. Regnier, A.J. Rivera, K.L. Kreutziger, and D.A. Martyn. 2004. Cardiac length dependence of force and force redevelopment kinetics with altered cross-bridge cycling. Biophys. J. 87:1784-1794. doi:10.1529/biophysj.103.039131
2. Backx, P.H. 1989. The force-sarcomere length relationship in rat cardiac muscle. PhD thesis. University of Calgary, Calgary, Canada. 116 pp.
3. 2+]i and cross-bridge kinetics. J. Physiol. 476:487-500.
4. Bell, S.P., J. Fabian, and M.M. LeWinter. 1998. Effects of dobutamine on left ventricular restoring forces. Am. J. Physiol. 275:H190-H194.
5. Bluhm, W.F., A.D. McCulloch, and W.Y. Lew. 1995. Active force in rabbit ventricular myocytes. J. Biomech. 28:1119-1122. doi:10.1016/ 0021-9290(94)00018-Y
6. Borbély, A., J. van der Velden, Z. Papp, J.G. Bronzwaer, I. Edes, G.J. Stienen, and W.J. Paulus. 2005. Cardiomyocyte stiffness in diastolic heart failure. Circulation. 111:774-781. doi:10.1161/01 .CIR.0000155257.33485.6D
7. Borbély, A., I. Falcao-Pires, L. van Heerebeek, N. Hamdani, I. Edes, C. Gavina, A.F. Leite-Moreira, J.G. Bronzwaer, Z. Papp, J. van der Velden, et al. 2009a. Hypophosphorylation of the stiff N2B titin isoform raises cardiomyocyte resting tension in failing human myocardium. Circ. Res. 104:780-786. doi:10.1161/ CIRCRESAHA.108.193326
8. Borbély, A., L. van Heerebeek, and W.J. Paulus. 2009b. Transcriptional and posttranslational modifications of titin: implications for diastole. Circ. Res. 104:12-14. doi:10.1161/CIRCRESAHA.108.191130 Brady, A.J. 1991. Mechanical properties of isolated cardiac myocytes. Physiol. Rev. 71:413-428.
9. Bronzwaer, J.G., and W.J. Paulus. 2005. Matrix, cytoskeleton, or myofilaments: which one to blame for diastolic left ventricular dysfunctioñ Prog. Cardiovasc. Dis. 47:276-284. doi:10.1016/j.pcad.2005.02. 003
10. Bub, G., P. Camelliti, C. Bollensdorff, D.J. Stuckey, G. Picton, R.A. Burton, K. Clarke, and P. Kohl. 2010. Measurement and analysis of sarcomere length in rat cardiomyocytes in situ and in vitro. Am. J. Physiol. Heart Circ. Physiol. 298:H1616-H1625. doi:10.1152/ajpheart.00481.2009
11. Fabiato, A., and F. Fabiato. 1979. Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J. Physiol. (Paris). 75:463-505.
12. Farman, G.P., J.S. Walker, P.P. de Tombe, and T.C. Irving. 2006. Impact of osmotic compression on sarcomere structure and myofilament calcium sensitivity of isolated rat myocardium. Am. J. Physiol. Heart Circ. Physiol. 291:H1847-H1855. doi:10.1152/ajpheart.01237.2005
13. Farman, G.P., K. Tachampa, R. Mateja, O. Cazorla, A. Lacampagne, and P.P. de Tombe. 2008. Blebbistatin: use as inhibitor of muscle contraction. Pflugers Arch. 455:995-1005. doi:10.1007/s00424- 007-0375-3
14. 2+-independent alterations in diastolic sarcomere length and relaxation kinetics in a mouse model of lipotoxic diabetic cardiomyopathy. Circ. Res. 104:95-103. doi:10.1161/ CIRCRESAHA.108.186809
15. 2+ sensitivity in intact versus skinned rat ventricular muscle. Circ. Res. 74:408-415.
16. Gao, W.D., N.G. Perez, and E. Marban. 1998. Calcium cycling and contractile activation in intact mouse cardiac muscle. J. Physiol. 507:175-184. doi:10.1111/j.1469-7793.1998.175bu.x
17. Granzier, H.L., and T.C. Irving. 1995. Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys. J. 68:1027-1044. doi:10.1016/S0006- 3495(95)80278-X
18. Granzier, H., M. Helmes, O. Cazorla, M. McNabb, D. Labeit, Y. Wu, R. Yamasaki, A. Redkar, M. Kellermayer, S. Labeit, and K. Trombitas. 2000. Mechanical properties of titin isoforms. Adv. Exp. Med. Biol. 481:283-300.
19. Hamdani, N., M. de Waard, A.E. Messer, N.M. Boontje, V. Kooij, S. van Dijk, A. Versteilen, R. Lamberts, D. Merkus, C. Dos Remedios, et al. 2008. Myofilament dysfunction in cardiac disease from mice to men. J. Muscle Res. Cell Motil. 29:189-201. doi:10.1007/s10974-008-9160-y
20. Harrison, S.M., and D.M. Bers. 1989. Influence of temperature on the calcium sensitivity of the myofilaments of skinned ventricular muscle from the rabbit. J. Gen. Physiol. 93:411-428.
21. Harrison, S.M., and D.M. Bers. 1990. Temperature dependence of myofilament Ca sensitivity of rat, guinea pig, and frog ventricular muscle. Am. J. Physiol. 258:C274-C281.
22. Helmes, M., K. Trombitás, and H. Granzier. 1996. Titin develops restoring force in rat cardiac myocytes. Circ. Res. 79:619-626.
23. Helmes, M., C.C. Lim, R. Liao, A. Bharti, L. Cui, and D.B. Sawyer. 2003. Titin determines the Frank-Starling relation in early diastole. J. Gen. Physiol. 121:97-110. doi:10.1085/jgp.20028652
24. Herrmann, C., J. Wray, F. Travers, and T. Barman. 1992. Effect of 2,3-butanedione monoxime on myosin and myofibrillar ATPases. An example of an uncompetitive inhibitor. Biochemistry. 31: 12227-12232. doi:10.1021/bi00163a036
25. Iribe, G., M. Helmes, and P. Kohl. 2007. Force-length relations in isolated intact cardiomyocytes subjected to dynamic changes in mechanical load. Am. J. Physiol. Heart Circ. Physiol. 292:H1487-H1497. doi:10.1152/ajpheart. 00909.2006
26. Irving, T.C., J. Konhilas, D. Perry, R. Fischetti, and P.P. de Tombe. 2000. Myofilament lattice spacing as a function of sarcomere length in isolated rat myocardium. Am. J. Physiol. Heart Circ. Physiol. 279:H2568-H2573.
27. Kass, D.A., J.G. Bronzwaer, and W.J. Paulus. 2004. What mechanisms underlie diastolic dysfunction in heart failure? Circ. Res. 94:1533-1542. doi:10.1161/01.RES.0000129254.25507.d6
28. Kentish, J.C., H.E. ter Keurs, L. Ricciardi, J.J. Bucx, and M.I. 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.
29. Kovács, M., J. Tóth, C. Hetényi, A. Málnási-Csizmadia, and J.R. Sellers. 2004. Mechanism of blebbistatin inhibition of myosin II. J. Biol. Chem. 279:35557-35563. doi:10.1074/jbc.M405319200
30. Krüger, M., and W.A. Linke. 2009. Titin-based mechanical signalling in normal and failing myocardium. J. Mol. Cell. Cardiol. 46:490-498. doi:10.1016/j.yjmcc.2009.01.004
31. Labeit, S., and B. Kolmerer. 1995. Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science. 270:293-296. doi: 10.1126/science.270.5234.293
32. Lahmers, S., Y. Wu, D.R. Call, S. Labeit, and H. Granzier. 2004. Developmental control of titin isoform expression and passive stiffness in fetal and neonatal myocardium. Circ. Res. 94:505-513. doi:10.1161/01.RES.0000115522. 52554.86
33. Le Guennec, J.Y., N. Peineau, J.A. Argibay, K.G. Mongo, and 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. doi:10.1016/0022-2828(90)90072-A
34. LeWinter, M.M., and H. Granzier. 2010. Cardiac titin: a multifunctional giant. Circulation. 121:2137-2145. doi:10.1161/ CIRCULATIONAHA.109.860171
35. LeWinter, M.M., J. Popper, M. McNabb, L. Nyland, S.B. Bell, and H. Granzier. 2010. Extensible behavior of titin in the miniswine left ventricle. Circulation. 121:768-774. doi:10.1161/ CIRCULATIONAHA.109.918151
36. Lorenzen-Schmidt, I., B.D. Stuyvers, H.E. ter Keurs, M.O. Date, M. Hoshijima, K.R. Chien, A.D. McCulloch, and J.H. Omens. 2005. Young MLP deficient mice show diastolic dysfunction before the onset of dilated cardiomyopathy. J. Mol. Cell. Cardiol. 39:241-250. doi:10.1016/j.yjmcc.2005.05.006
37. Nash, G.B., P.E. Tatham, T. Powell, V.W. Twist, R.D. Speller, and L.T. Loverock. 1979. Size measurements on isolated rat heart cells using Coulter analysis and light scatter flow cytometry. Biochim. Biophys. Acta. 587:99-111.
38. Neagoe, C., C.A. Opitz, I. Makarenko, and W.A. Linke. 2003. Gigantic variety: expression patterns of titin isoforms in striated muscles and consequences for myofibrillar passive stiffness. J. Muscle Res. Cell Motil. 24:175-189. doi:10.1023/ A:1026053530766
39. Niggli, E. 1988. A laser diffraction system with improved sensitivity for long-time measurements of sarcomere dynamics in isolated cardiac myocytes. Pflugers Arch. 411:462-468. doi:10.1007/ BF00587728
40. Nishimura, R.A., and W. Jaber. 2007. Understanding "diastolic heart failure": the tip of the iceberg. J. Am. Coll. Cardiol. 49:695-697. doi:10.1016/j.jacc.2006.11.014
41. O'Connell, T.D., M.C. Rodrigo, and P.C. Simpson. 2007. Isolation and culture of adult mouse cardiac myocytes. Methods Mol. Biol. 357:271-296.
42. Owan, T.E., D.O. Hodge, R.M. Herges, S.J. Jacobsen, V.L. Roger, and M.M. Redfield. 2006. Trends in prevalence and outcome of heart failure with preserved ejection fraction. N. Engl. J. Med. 355:251-259. doi:10.1056/NEJMoa052256
43. Preetha, N., W. Yiming, M. Helmes, F. Norio, L. Siegfried, and H. Granzier. 2005. Restoring force development by titin/connectin and assessment of Ig domain unfolding. J. Muscle Res. Cell Motil. 26:307-317. doi:10.1007/s10974-005-9037-2
44. Roos, K.P., and A.J. Brady. 1989. Stiffness and shortening changes in myofilament-extracted rat cardiac myocytes. Am. J. Physiol. 256:H539-H551.
45. 2+. J. Physiol. 502:661-677. doi:10.1111/j.1469- 7793.1997.661bj.x
46. Stuyvers, B.D., A.D. McCulloch, J. Guo, H.J. Duff, and H.E. ter Keurs. 2002. Effect of stimulation rate, sarcomere length and Ca(2+) on force generation by mouse cardiac muscle. J. Physiol. 544:817-830. doi:10.1113/jphysiol.2002.024430
47. Ter Keurs, H.E., T. Shinozaki, Y.M. Zhang, Y. Wakayama, Y. Sugai, Y. Kagaya, M. Miura, P.A. Boyden, B.D. Stuyvers, and A. Landesberg. 2008. Sarcomere mechanics in uniform and nonuniform cardiac muscle: a link between pump function and arrhythmias. Ann. NY Acad. Sci. 1123:79-95. doi:10.1196/annals. 1420.010
48. Trombitás, K., and H. Granzier. 1997. Actin removal from cardiac myocytes shows that near Z line titin attaches to actin while under tension. Am. J. Physiol. 273:C662-C670.
49. Trombitás, K., A. Freiburg, M. Greaser, S. Labeit, and H. Granzier. 2000. From connecting filaments to co-expression of titin isoforms. Adv. Exp. Med. Biol. 481:405-418.
50. Trombitás, K., Y. Wu, D. Labeit, S. Labeit, and H. Granzier. 2001. Cardiac titin isoforms are coexpressed in the half-sarcomere and extend independently. Am. J. Physiol. Heart Circ. Physiol. 281:H1793-H1799.
51. Warren, C.M., P.R. Krzesinski, and M.L. Greaser. 2003. Vertical agarose gel electrophoresis and electroblotting of high-molecular-weight proteins. Electrophoresis. 24:1695-1702. doi:10.1002/elps.200305392
52. Wussling, M., W. Schenk, and B. Nilius. 1987. A study of dynamic properties in isolated myocardial cells by the laser diffraction method. J. Mol. Cell. Cardiol. 19:897-907. doi:10.1016/ S0022-2828(87)80618-1
53. Yasuda, S.I., S. Sugiura, N. Kobayakawa, H. Fujita, H. Yamashita, K. Katoh, Y. Saeki, H. Kaneko, Y. Suda, R. Nagai, and H. Sugi. 2001. A novel method to study contraction characteristics of a single cardiac myocyte using carbon fibers. Am. J. Physiol. Heart Circ. Physiol. 281:H1442-H1446.
54. Yasuda, S., D. Townsend, D.E. Michele, E.G. Favre, S.M. Day, and J.M. Metzger. 2005. Dystrophic heart failure blocked by membrane sealant poloxamer. Nature. 436:1025-1029. doi:10.1038/ nature03844
55. Zile, M.R., and D.L. Brutsaert. 2002a. New concepts in diastolic dysfunction and diastolic heart failure: part I: diagnosis, prognosis, and measurements of diastolic function. Circulation. 105:1387-1393. doi:10.1161/hc1102.105289
56. Zile, M.R., and D.L. Brutsaert. 2002b. New concepts in diastolic dysfunction and diastolic heart failure: part II: causal mechanisms and treatment. Circulation. 105:1503-1508. doi:10.1161/ hc1202.105290