The Frank-Starling mechanism in vertebrate cardiac myocytes

Journal of Experimental Biology

Volumn 211, Issue 13, 2008, Pages 2005-2013

  Shiels, Holly A ^a   White, Ed ^b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Amphibians; Birds; Fish; Mammals; Reptiles; Sarcomere length tension relationship

Indexed keywords

TROPONIN;

ANIMAL; BIOLOGICAL MODEL; BIOMECHANICS; CALCIUM SIGNALING; CLASSIFICATION; COMPARATIVE STUDY; HEART CONTRACTION; HEART MUSCLE CELL; HEART OUTPUT; HEART STROKE VOLUME; MAMMAL; MICROFILAMENT; NOTE; PHYSIOLOGY; SARCOMERE; VERTEBRATE;

ANIMALS; BIOMECHANICS; CALCIUM SIGNALING; CARDIAC OUTPUT; MAMMALS; MICROFILAMENTS; MODELS, CARDIOVASCULAR; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; SARCOMERES; STROKE VOLUME; TROPONIN; VERTEBRATES;

AMPHIBIA; AVES; MAMMALIA; REPTILIA; VERTEBRATA;

EID: 47949122658     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.003145     Document Type: Note

References (85)

1. Allen, D. G. and Blinks, J. R. (1978). Calcium transients in aequorin-injected frog cardiac muscle. Nature 273, 509-513.
2. Allen, D. and Kentish, J. (1985). The cellular basis of the length-tension relation in cardiac muscle. J. Mol. Cell. Cardiol. 9, 821-840.
3. Allen, D. G. and Kurihara, S. (1982). The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J. Physiol. 327, 79-94.
4. Asnes, C. F., Marquez, J. P., Elson, E. L. and Wakatsuki, T. (2006). Reconstitution of the Frank-Starling mechanism in engineered heart tissues. Biophys. J. 91, 1800-1810.
5. Axelsson, M., Davison, W., Forster, M. E. and Farrell, A. P. (1992). Cardiovascular responses of the red-blooded Antarctic fishes Pagothenia bernacchii and P. borchgrevinki. J. Exp. Biol. 167, 179-201.
6. Bean, B. P., Nowycky, M. C. and Tsien, R. W. (1984). β-Adrenergic modulation of calcium channels in frog ventricular heart cells. Nature 307, 371-375.
7. Bers, D. M. (2002). Cardiac excitation-contraction coupling. Nature 415, 198-205.
8. 2+ on the hearts of yellowfin tuna (Thunnus albacares). J. Exp. Biol. 205, 1881-1888.
9. Burggren, W., Farrell, A. and Lillywhite, H. (1997). Vertebrate cardiovascular systems. In The Handbook of Physiology (ed. W. H. Dantzler), pp. 215-308. New York, Oxford: Oxford University Press.
10. Burggren, W., Khorrami, S., Pinder, A. and Sun, T. (2004). Body, eye, and chorioallantoic vessel growth are not dependent on cardiac output level in day 3-4 chicken embryos. Am. J. Physiol. 287, R1399-R1406.
11. Butler, P. J., Frappell, P. B., Wang, T. and Wikelski, M. (2002). The relationship between heart rate and rate of oxygen consumption in Galapagos marine iguanas (Amblyrhynchus cristatus) at two different temperatures. J. Exp. Biol. 205, 1917-1924.
12. + exchange and stretch-activated channels underlies the slow inotropic response to stretch in myocytes and muscle from the rat heart. J. Physiol. 559, 205-214.
13. Cazoria, O., Pascarel, C., Garnier, D. and Le Guennec, J. (1997). Resting tension participates in the modulation of active tension in isolated guinea pig ventricular myocytes. J. Mol. Cell. Cardiol. 29, 1629-1637.
14. Cazoria, O., Le Guennec, J. Y. and White, E. (2000a). Length-tension relationships of sub-epicardial and sub-endocardial single ventricular myocytes from rat and ferret hearts. J. Mol. Cell. Cardiol. 32, 735-744.
15. Cazoria, O., Freiburg, A., Helmes, M., Centner, T., McNabb, M., Wu, Y., Trombitas, K., Labeit, S. and Granzier, H. (2000b). Differential expression of cardiac titin isoforms and modulation of cellular stiffness. Circ. Res. 86, 59-67.
16. Cazoria, O., Wu, Y., Irving, T. C. and Granzier, H. (2001). Titin-based modulation of calcium sensitivity of active tension in mouse skinned cardiac myocytes. Circ. Res. 88, 1028-1035.
17. Cazoria, O., Szilagyi, S., Le Guennec, J. Y., Vassort, G. and Lacampagne, A. (2005). Transmural stretch-dependent regulation of contractile properties in rat heart and its alteration after myocardial infarction. FASEB J. 19, 88-90.
18. 2+ sensitivity of cardiac myofibrils: a comparison of trout with mammals. Am. J. Physiol. 267, R62-R70.
19. Fabiato, A. and Fabiato, F. (1975). Dependence of the contractile activation of skinned cardiac cells on the sarcomere length. Nature 256, 54-56.
20. Fabiato, A. and Fabiato, F. (1978a). Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiac and skeletal muscles. J. Physiol. 276, 233-255.
21. Fabiato, A. and Fabiato, F. (1978b). Myofilament-generated tension oscillations during partial calcium activation and activation dependence of the sarcomere length-tension relation of skinned cardiac cells. J. Gen. Physiol. 72, 667-699.
22. Farrell, A. P. (1991). From hagfish to tuna: a perspective on cardiac-function in fish. Physiol. Biochem. Zool. 64, 1137-1164.
23. Farrell, A. P. (2007). Tribute to P. L. Lutz: a message from the heart - why hypoxic bradycardia in fishes? J. Exp. Biol. 210, 1715-1725.
24. Farrell, A. P. and Jones, D. R. (1992). The Heart. In The Cardiovascular System. Vol. XIIA (ed. W. S. Hoar, D. J. Randall and A. P. Farrell), pp. 1-88. San Diego: Academic Press.
25. Farrell, A. P., MacLeod, K. and Chancey, B. (1986). Intrinsic mechanical properties of the perfused rainbow trout heart and the effects of catecholamines and extracellular calcium under control and acidotic conditions. J. Exp. Biol. 125, 319-345.
26. Farrell, A., Franklin, C., Arthur, P., Thorarensen, H. and Cousins, K. (1994). Mechanical performance of an in situ perfused heart from the turtle chrysemys scripta during normoxia and anoxia at 5°C and 15°C. J. Exp. Biol. 191, 207-229.
27. 2+ activation of rat ventricular myocytes. Circ. Res. 83, 602-607.
28. Franklin, C. E. (1994). Intrinsic properties of an in situ turtle heart (Emydura signata) preparation perfused via both atria. Comp. Biochem. Physiol. 107, 501-507.
29. Franklin, C. and Axelsson, M. (1994). The intrinsic properties of an in situ perfused crocodile heart. J. Exp. Biol. 186, 269-288.
30. Franklin, C. E. and Davie, P. S. (1992). Dimensional analysis of the ventricle of an in situ perfused trout heart using echocardiography. J. Exp. Biol. 166, 47-60.
31. Frappell, P., Schultz, T. and Christian, K. (2002). Oxygen transfer during aerobic exercise in a varanid lizard Varanus mertensi is limited by the circulation. J. Exp. Biol. 205, 2725-2736.
32. 2+ binding. J. Mol. Cell. Cardiol. 28, 1375-1383.
33. Fujita, H., Labeit, D., Gerull, B., Labeit, S. and Granzier, H. L. (2004). Titin isoform-dependent effect of calcium on passive myocardial tension. Am. J. Physiol. 287, H2528-H2534.
34. Fukuda, N. and Granzier, H. (2005). Titin/connectin-based modulation of the Frank-Starling mechanism of the heart. J. Muscle Res. Cell Motil. 26, 319-323.
35. Fukuda, N., Sasaki, D., Ishiwata, S. and Kurihara, S. (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.
36. Fukuda, N., Wu, Y., Farman, G., Irving, T. C. and Granzier, H. (2005a). Titin-based modulation of active tension and interfilament lattice spacing in skinned rat cardiac muscle. Pflügers Arch. 449, 449-457.
37. Fukuda, N., Wu, Y., Nair, P. and Granzier, H. L. (2005b). Phosphorylation of titin modulates passive stiffness of cardiac muscle in a titin isoform-dependent manner. J. Gen. Physiol. 125, 257-271.
38. Galli, G. L., Taylor, E. W. and Shiels, H. A. (2006). Calcium flux in turtle ventricular myocytes. Am. J. Physiol. 291, R1781-R1789.
39. Gilbert, S. F., Benson, A., Li, P. F., Holden, A. V., Wakabayashi, K. F., Sugimoto, Y. F., Tanaka, H. F., Ueno, Y. F., Takezawa, Y. F. and Amemiya, Y. (2007). Regional localisation of left ventricular sheet structure: integration with current models of cardiac fibre, sheet and band structure: x-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Eur. J. Cardiothorac. Surg. 32, 231-249.
40. 2+ binding to cardiac troponin C: effects of temperature and pH on mammalian and salmonid isoforms. Am. J. Physiol. 279, R1707-R1715.
41. 2+ affinity of site II. Am. J. Physiol. 284, C1176-C1184.
42. Gillis, T. E., Martyn, D. A., Rivera, A. J. and Regnier, M. (2007). Investigation of thin filament near-neighbour regulatory unit interactions during force development in skinned cardiac and skeletal muscle. J. Physiol. 580, 561-576.
43. Gleeson, T. T., Mitchell, G. S. and Bennett, A. F. (1980). Cardiovascular responses to graded activity in the lizards Varanus and Iguana. Am. J. Physiol. 239, R174-R179.
44. 2+ current in single frog ventricular myocytes. J. Physiol. 530, 79-91.
45. Gordon, A. and Ridgway, E. (1993). Cross-bridges affect both TnC structure and calcium affinity in muscle fibers. Adv. Exp. Med. Biol. 332, 183-192.
46. Gordon, A. M., Huxley, A. F. and Julian, F. J. (1966). The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J. Physiol. 184, 170-192.
47. Gordon, A. M., Regnier, M. and Homsher, E. (2001). Skeletal and cardiac muscle contractile activation: tropomyosin "rocks and rolls". News Physiol. Sci. 16, 49-55.
48. Granzier, H. and Labeit, S. (2002). Cardiac titin: an adjustable multi-functional spring. J. Physiol. 541, 335-342.
49. Granzier, H. L. and Labeit, S. (2004). The giant protein titin: a major player in myocardial mechanics, signalling, and disease. Circ. Res. 94, 284-295.
50. Grubb, B. R. (1982). Cardiac output and stroke volume in exercising ducks and pigeons. J. Appl. Physiol. 53, 207-211.
51. Harrison, S. M. and Bers, D. M. (1990). Temperature dependence of myofilament Ca sensitivity of rat, guinea pig, and frog ventricular muscle. Am. J. Physiol. 258, C274-C281.
52. Hedrick, M. S., Palioca, W. B. and Hillman, S. S. (1999). Effects of temperature and physical activity on blood flow shunts and intracardiac mixing in the toad Bufo marinus. Physiol. Biochem. Zool. 72, 509-519.
53. Jewett, P. H., Sommer, J. R. and Johnson, E. A. (1971). Cardiac muscle. Its ultrastructure in the finch and hummingbird with special reference to the sarcoplasmic reticulum. J. Cell Biol. 49, 50-65.
54. Jones, D. R. and Randall, D. J. (1978). The respiratory and circulatory systems during exercise. In Fish Physiology (ed. W. S. Hoar and D. J. Randall), pp. 425-501. New York: Academic Press.
55. Kentish, J. C., ter Keurs, H. E., Ricciardi, L., Bucx, J. J. and Noble, M. I. (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.
56. Kim, C. S., Davidoff, A. J., Maki, T. M., Doye, A. A. and Gwathmey, J. K. (2000). Intracellular calcium and the relationship to contractility in an avian model of heart failure. J. Comp. Physiol. B 170, 295-306.
57. Konhilas, J. P., Irving, T. and de Tombe, P. (2002a). Frank-Starling law of the heart and the cellular mechanisms of length-dependent activation. Pflügers Arch. 445, 305-310.
58. Konhilas, J. P., Irving, T. C. and de Tombe, P. P. (2002b). Myofilament calcium sensitivity in skinned rat cardiac trabeculae: role of interfilament spacing. Circ. Res. 90, 59-65.
59. Konhilas, J. P., Irving, T. C., Wolska, B. M., Jweied, E. E., Martin, A. F., Solaro, R. J. and Tombe, P. P. (2003). Troponin I in the murine myocardium: influence on length-dependent activation and interfilament spacing. J. Physiol. 547, 951-961.
60. Korsmeyer, K. E., Lai, N. C., Shadwick, R. E. and Graham, J. B. (1997). Heart rate and stroke volume contribution to cardiac output in swimming yellowfin tuna: response to exercise and temperature. J. Exp. Biol. 200, 1975-1986.
61. Lillywhite, H. B., Zippel, K. C. and Farrell, A. P. (1999). Resting and maximal heart rates in ectothermic vertebrates. Comp. Biochem. Physiol. 124A, 369-382.
62. McKean, T., Scherzer, A. and Park, H. (1997). Hypoxia and ischaemia in buffer-perfused toad hearts. J. Exp. Biol. 200, 2575-2581.
63. McKean, T., Li, G. and Wei, K. (2002). Cardiac effects of hypoxia in the neotenous tiger salamander Ambystoma tigrinum. J. Exp. Biol. 205, 1725-1734.
64. Mendonça, P. C., Genge, A. G., Deitch, E. J. and Gamperi, A. K. (2007). Mechanisms responsible for the enhanced pumping capacity of the in situ winter flounder heart (Pseudopleuronectes americanus). Am. J. Physiol. 293, R2112-R2119.
65. Neagoe, C., Opitz, C. A., Makarenko, I. and Linke, W. A. (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.
66. Page, S. G. (1974). Measurement of structural parameters in cardiac muscle. In The Physiological Basis of Starling's Law of the Heart (ed. R. Porter and D. W. Fitzsimons), pp. 13-30. Amsterdam: Elsevier.
67. Palmer, B. M., Noguchi, T., Wang, Y., Heim, J. R., Alpert, N. R., Burgon, P. G., Seidman, C. E., Seidman, J. G., Maughan, D. W. and LeWinter, M. M. (2004). Effect of cardiac myosin binding protein-C on mechanoenergetics in mouse myocardium. Circ. Res. 94, 1615-1622.
68. Peters, G. W., Steiner, D. A., Rigoni, J. A., Mascilli, A. D., Schnepp, R. W. and Thomas, S. P. (2005). Cardiorespiratory adjustments of homing pigeons to steady wind tunnel flight. J. Exp. Biol. 208, 3109-3120.
69. Robinson, T. and Winegrad, S. (1979). The measurement and dynamic implications of thin filament lengths in heart muscle. J. Physiol. 286, 607-619.
70. Satoh, H., Delbridge, L. M., Blatter, L. A. and Bers, D. M. (1996). Surface:volume relationship in cardiac myocytes studied with confocal microscopy and membrane capacitance measurements: species-dependence and developmental effects. Biophys. J. 70, 1494-1504.
71. Seeley, M., Huang, W., Chen, Z., Wolff, W. O., Lin, X. and Xu, X. (2007). Depletion of zebrafish titin reduces cardiac contractility by disrupting the assembly of Z-discs and A-bands. Circ. Res. 100, 238-245.
72. 2+ flux in trout ventricular myocytes. Am. J. Physiol. 288, R1756-R1766.
73. Shiels, H. and White, E. (2007). The effect of mechanical stimulation on vertebrate hearts: a question of class. In Mechanosensitive Ion Channels (ed. A. Kamkin and I. Kiseleva), pp. 331-350. New York: Springer.
74. Shiels, H. A., Calaghan, S. C. and White, E. (2006). The cellular basis for enhanced volume-modulated cardiac output in fish hearts. J. Gen. Physiol. 128, 37-44.
75. Stevens, C. F. and Hunter, P. J. (2003). Sarcomere length changes in a 3D mathematical model of the pig ventricles. Prog. Biophys. Mol. Biol. 82, 229-241.
76. Sweeney, H. L., Bowman, B. F. and Stull, J. T. (1993). Myosin light chain phosphorylation in vertebrate straited muscle: regulation and function. Am. J. Physiol. 264, C1085-C1095.
77. Syme, D. A. and Josephson, R. T. (1995). Influence of muscle length on work from trabecular muscle of frog atrium and ventricle. J. Exp. Biol. 198, 2221-2227.
78. Tachampa, K., Wang, H., Farman, G. P. and de Tombe, P. P. (2007). Cardiac troponin I threonine 144, role in myofilament length dependent activation. Circ. Res. 101, 1081-1083.
79. Tarr, M., Trank, J. W., Goertz, K. K. and Leiffer, P. (1981). Effect of initial sarcomere length on sarcomere kinetics and force development in single frog atrial cardiac cells. Circ. Res. 49, 767-774.
80. Tibbits, G. F., Hove-Madsen, L. and Bers, D. M. (1991). Calcium-transport and the regulation of cardiac contractility in teleosts: a comparison with higher vertebrates. Can. J. Zool. 69, 2014-2019.
81. 2+ current in fish cardiac myocytes: effects of thermal acclimation and beta-adrenergic stimulation. J. Exp. Biol. 201, 533-547.
82. Wakabayashi, K., Sugimoto, Y., Tanaka, H., Ueno, Y., Takezawa, Y. and Amemiya, Y. (1994). X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys. J. 67, 2422-2435.
83. Wang, T., Altimiras, J. and Axelsson, M. (2002). Intracardiac flow separation in an in situ perfused heart from Burmese python Python molurus. J. Exp. Biol. 205, 2715-2723.
84. Wu, Y., Cazoria, O., Labeit, D. and Granzier, H. (2000). Changes in titin and collagen underlie diastolic stiffness diversity of cardiac muscle. J. Mol. Cell. Cardiol. 32, 2151-2162.
85. Wu, Y., Tobias, A. H., Bell, K., Barry, W., Helmes, M., Trombitas, K., Tucker, R., Campbell, K. B. and Granzier, H. L. (2004). Cellular and molecular mechanisms of systolic and diastolic dysfunction in an avian model of dilated cardiomyopathy. J. Mol. Cell. Cardiol. 37, 111-119.