Sarcomere strain and heterogeneity correlate with injury to frog skeletal muscle fiber bundles

Journal of Applied Physiology

Volumn 97, Issue 5, 2004, Pages 1803-1813

  Patel, Tina J ^a   Das, Ronnie ^a   Fridén, Jan ^b   Lutz, Gordon J ^c   Lieber, Richard L ^a,d  

^a VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^b SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^c DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Cytoskeleton; Eccentric contraction; Laser diffraction; Mechanics

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL HETEROGENEITY; CONTROLLED STUDY; CORRELATION ANALYSIS; FAST MUSCLE FIBER; FROG; LASER DIFFRACTION; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE INJURY; NONHUMAN; PRIORITY JOURNAL; SARCOMERE; SARCOMERE LENGTH; SKELETAL MUSCLE; STATISTICAL SIGNIFICANCE; STRAIN DIFFERENCE; STRESS STRAIN RELATIONSHIP; TIBIALIS ANTERIOR MUSCLE;

ANIMALS; MUSCLE CONTRACTION; MUSCLE FIBERS; MUSCLE, SKELETAL; MYOSIN HEAVY CHAINS; RANA PIPIENS; RANDOM ALLOCATION; SARCOMERES; STRESS, MECHANICAL; WOUNDS AND INJURIES;

EID: 7044269334     PISSN: 87507587     EISSN: None     Source Type: Journal    
DOI: 10.1152/japplphysiol.00505.2003     Document Type: Article

References (72)

1. Altringham JD and Bottinelli R. The descending limb of the sarcomere length-force relation in single muscle fibers of the frog. J Muscle Res Cell Motil 6: 585-600, 1985.
2. Bahler AS, Fales JT, and Zierler KL. The dynamic properties of mammalian skeletal muscle. J Gen Physiol 51: 369-384, 1968.
3. Balnave CD and Allen DG. Intracellular calcium and force in single mouse muscle fibres following repeated contractions with stretch. J Physiol 488: 25-36, 1995.
4. Banes AJ. Mechanical strain and the mammalian cell. In: Physical Forces and the Mammalian Cell, edited by Frangos JA. San Diego, CA: Academic, 1993, p. 81-123.
5. Baskin RJ, Lieber RL, Oba T, and Yeh Y. Intensity of light diffraction from striated muscle as a function of incident angle. Biophys J 36: 759-773, 1981.
6. Benz RJ, Fridén J, and Lieber RL. Simultaneous stiffness and force measurements reveal subtle injury to rabbit soleus muscles. Mol Cell Biochem 122: 312-319, 1998.
7. Brooks SV, Zerba E, and Faulkner JA. Injury to muscle fibres after single stretches of passive and maximally stimulated muscles in mice. J Physiol 488: 459-469, 1995.
8. Brown LM and Hill L. Some observations on variations in filament overlap in tetanized muscle fibres and fibres stretched during a tetanus, detected in the electron microscope after rapid fixation. J Muscle Res Cell Motil 12: 171-182, 1991.
9. Burkholder TJ and Lieber RL. Sarcomere length operating range of muscles during movement. J Exp Biol 204: 1529-1536, 2001.
10. Cleworth DR and Edman K. Changes in sarcomere length during isometric tension development in frog skeletal muscle. J Physiol 227: 1-17, 1972.
11. Close RI. The relations between sarcomere length and characteristics of isometric twitch contractions of frog sartorius muscle. J Physiol 220: 745-762, 1972.
12. Edman K. The relation between sarcomere length and active tension in isolated semitendinosus fibres of the frog. J Physiol 183: 407-417, 1966.
13. Edman K, Mulieri LA, and Scubon MB. Non-hyperbolic force-velocity relationship in single muscle fibres. Acta Physiol Scand 98: 143-156, 1976.
14. Evans WJ, Meredith CN, Cannon JG, Dinarello CA, Frontera WR, Hughes VA, Jones BH, and Knuttgen HG. Metabolic changes following eccentric exercise in trained and untrained men. J Appl Physiol 61: 1864-1868, 1986.
15. Fridén J, Sjö'ström M, and Ekblom B. A morphological study of delayed muscle soreness. Experientia 37: 506-507, 1981.
16. Fridén J, Sjöström M, and Ekblom B. Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med 4: 170-176, 1983.
17. Fujime S. Optical diffraction study of muscle fibers. Biochim Biophys Acta 379: 227-238, 1975.
18. Garrett WE Jr, Safran MR, Seaber AV, Glisson RR, and Ribbeck BM. Biomechanical comparison of stimulated and nonstimulated skeletal muscle pulled to failure. Am J Sports Med 15: 448-454, 1987.
19. Gordon AM, Huxley AF, and Julian FJ. Tension development in highly stretched vertebrate muscle fibres. J Physiol 184: 143-169, 1966.
20. Gordon AM, Huxley AF, and Julian FJ. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol 184: 170-192, 1966.
21. Guharay F and Sachs F. Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. J Physiol 352: 685-701, 1984.
22. Harry JD, Ward AW, Heglund NC, Morgan DL, and McMahon TA. Cross-bridge cycling theories cannot explain high-speed lengthening behavior in frog muscle. Biophys J 57: 201-208, 1990.
23. Hill DK. Tension due to interaction between the sliding filaments in resting striated muscle. The effect of stimulation. J Physiol 199: 637-684, 1968.
24. Huxley AF. Muscle structure and theories of contraction. Prog Biophys Mol Biol 1: 255-318, 1957.
25. Ingber DE. Fibronectin controls capillary endothelial cell growth by modulating cell shape. Proc Natl Acad Sci USA 87: 3579-3583, 1990.
26. Julian FJ and Morgan DL. The effect on tension of non-uniform distribution of length changes applied to frog muscle fibres. J Physiol 293: 379-392, 1979.
27. Julian FJ and Morgan DL. Intersarcomere dynamics during fixed end tetanic contractions of frog muscle fibers. J Physiol 293: 365-378, 1979.
28. Katz B. The relation between force and speed in muscular contraction. J Physiol 96: 45-64, 1939.
29. Kawai M and Kunz ID. Optical diffraction studies of muscle fibers. Biophys J 13: 857-876, 1973.
30. Kawakami Y and Lieber RL. Interaction between series compliance and sarcomere kinetics determines internal sarcomere shortening during fixed-end contraction. J Biomech 33: 1249-1255, 2000.
31. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685, 1970.
32. Lännergren J. Contractile properties and myosin isoenzymes of various kinds of Xenopus twitch muscle fibres. J Muscle Res Cell Motil 8: 260-273, 1987.
33. Lännergren J and Hoh JFY. Myosin isozymes in single muscle fibers of Xenopus laevis: analysis of five different functional types. Proc R Soc Lond B Biol Sci 222: 401-408, 1984.
34. Leung AF. Calculation of the laser diffraction intensity of striated muscle by numerical methods. Comput Programs Biomed 15: 169-174, 1982.
35. Lieber RL and Baskin RJ. Intersarcomere dynamics of single muscle fibers during fixed-end tetani. J Gen Physiol 82: 347-364, 1983.
36. Lieber RL and Fridén J. Selective damage of fast glycolytic muscle fibers with eccentric contraction of the rabbit tibialis anterior. Acta Physiol Scand 133: 587-588, 1988.
37. Lieber RL and Fridén J. Muscle damage is not a function of muscle force but active muscle strain. J Appl Physiol 74: 520-526, 1993.
38. Lieber RL, Leonard ME, Brown CG, and Trestik CL. Frog semitendinosus tendon load-strain and stress-strain properties during passive loading. Am J Physiol Cell Physiol 261: C86-C92, 1991.
39. Lieber RL, McKee-Woodburn T, and Fridén J. Muscle damage induced by eccentric contractions of 25% strain. J Appl Physiol 70: 2498-2507, 1991.
40. Lieber RL, Thornell LE, and Fridén J. Muscle cytoskeletal disruption occurs within the first 15 minutes of cyclic eccentric contraction. J Appl Physiol 80: 278-284, 1996.
41. Lieber RL, Yeh Y, and Baskin RJ. Sarcomere length determination using laser diffraction. Effect of beam and fiber diameter. Biophys J 45: 1007-1016, 1984.
42. Lutz GJ, Bremner SN, and Lieber RL. Identification of myosin light chains in Rana pipiens skeletal muscle and their expression patterns along single fibers. J Exp Biol 204: 4237-4248, 2002.
43. Lutz GJ, Cuizon DB, Ryan AF, and Lieber RL. Four novel myosin heavy chain transcripts in Rana pipiens single muscle fibres define a molecular basis for muscle fibre types in the frog. J Physiol 508: 667-680, 1998.
44. Lutz GJ, Sirsi SR, Shapard-Palmer SA, Bremner SN, and Lieber RL. Influence of myosin isoforms on contractile properties of intact muscle fibers from Rana pipiens. Am J Physiol Cell Physiol 282: C835-C844, 2002.
45. Lynch GS and Faulkner JA. Contraction-induced injury to single muscle fibers: velocity of stretch does not influence the force deficit. Am J Physiol Cell Physiol 275: C1548-C1554, 1998.
46. Lynn R and Morgan DL. Decline running produces more sarcomeres in rat vastus intermedius muscle fibers than does incline running. J Appl Physiol 77: 1439-1444, 1994.
47. Macpherson PC, Dennis RG, and Faulkner JA. Sarcomere dynamics and contraction-induced injury to maximally activated single muscle fibres from soleus muscles of rats. J Physiol 500: 523-533, 1997.
48. Marikhin VA and Myasnikova LP. [Light diffraction by muscle fibers. I. Analysis of the geometric pattern of diffraction.] Tsitologiia 12: 1231-1236, 1970.
49. McCully KK and Faulkner JA. Injury to skeletal muscle fibers of mice following lengthening contractions. J Appl Physiol 59: 119-126, 1985.
50. Mendez J and Keys A. Density and composition of mammalian muscle. Metabolism 9: 184-188, 1960.
51. Morgan DL. Predictions of some effects on light diffraction patterns of muscles produced by areas with different sarcomere lengths (Abstract). Biophys J 21: 88a, 1978.
52. Morgan DL. New insights into the behavior of muscle during active lengthening. Biophys J 57: 209-221, 1990.
53. Morgan DL and Allen DG. Early events in stretch-induced muscle damage. J Appl Physiol 87: 2007-2015, 1999.
54. Morgan DL, Claflin DR, and Julian FJ. The effects of repeated active stretches on tension generation and myoplasmic calcium in frog single muscle fibres. J Physiol 497: 665-674, 1996.
55. Oba T, Baskin RJ, and Lieber RL. Light diffraction studies of active muscles fibres as a function of sarcomere length. J Muscle Res Cell Motil 2: 215-224, 1981.
56. Paolini PJ and Roos KP. Length-dependent optical diffraction pattern changes in frog sartorius muscle. Physiol Chem Phys 7: 235-254, 1975.
57. Paolini PJ, Roos KP, and Baskin RJ. Light diffraction studies of sarcomere dynamics in single skeletal muscle fibers. Biophys J 20: 221-232, 1977.
58. Proske U and Morgan DL. Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol 537: 333-345, 2001.
59. Rüdel R and Zite-Ferenczy F. Interpretation of light diffraction by cross-striated muscle as Bragg reflexion of light by the lattice of contractile proteins. J Physiol 290: 317-330, 1979.
60. Sam M, Shah S, Fridén J, Milner DJ, Capetanaki Y, and Lieber RL. Desmin knockout muscles generate lower stress and are less vulnerable to injury compared to wild-type muscles. Am J Physiol Cell Physiol 279: C1116-C1122, 2000.
61. Sandow A. Diffraction patterns of the frog sartorius and sarcomere behavior during contraction. J Cell Comp Physiol 9: 55-75, 1936.
62. Sandow A. Diffraction patterns of the frog sartorius and sarcomere behavior under stretch. J Cell Comp Physiol 9: 37-54, 1936.
63. Sokal RR and Rohlf FJ. Biometry. San Francisco, CA: Freeman, 1981.
64. Stauber WT, Fritz VK, Vogelbach DW, and Dahlmann B. Characterization of muscles injured by forced lengthening. I. Cellular infiltrates. Med Sci Sports Exerc 20: 345-353, 1988.
65. Talbot JA and Morgan DL. Quantitative analysis of sarcomere nonuniformities in active muscle following a stretch. J Muscle Res Cell Motil 17: 261-268, 1996.
66. Talmadge RJ and Roy RM. Elecrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J Appl Physiol 75: 2337-2340, 1993.
67. Trestik CL and Lieber RL. Relationship between achilles tendon mechanical properties and gastrocnemius muscle function. J Biomech Eng 115: 225-230, 1993.
68. Warren GL, Lowe DA, Hayes DA, Karwoski CJ, Prior BM, and Armstrong RB. Excitation failure in eccentric contraction-induced injury of mouse soleus muscle. J Physiol 468: 487-499, 1993.
69. Warren GW, Hayes D, Lowe DA, and Armstrong RB. Mechanical factors in the initiation of eccentric contraction-induced injury in rat soleus muscle. J Physiol 464: 457-475, 1993.
70. Whitehead NP, Allen TJ, Morgan DL, and Proske U. Damage to human muscle from eccentric exercise after training with concentric exercise. J Physiol 512: 615-620, 1998.
71. Wood SA, Morgan DL, and Proske U. Effects of repeated eccentric contractions on structure and mechanical properties of toad sartorius muscle. Am J Physiol Cell Physiol 265: C792-C800, 1993.
72. Yeh Y, Baskin RJ, Lieber RL, and Roos KP. Theory of light diffraction by single skeletal muscle fibers. Biophys J 29: 509-522, 1980.