Abstract
The myofibrillar and cytoskeletal alterations observed in delayed onset muscle soreness (DOMS) caused by eccentric exercise are generally considered to represent damage. By contrast our recent immunohistochemical studies suggested that the alterations reflect myofibrillar remodeling (Yu and Thornell 2002; Yu et al. 2003). In the present study the same human muscle biopsies were further analyzed with transmission electron microscopy and immunoelectron microscopy. We show that the ultrastructural hallmarks of DOMS, Z-disc streaming, Z-disc smearing, and Z-disc disruption were present in the biopsies and were significantly more frequent in biopsies taken 2–3 days and 7–8 days after exercise than in those from controls and 1 h after exercise. Four main types of changes were observed: amorphous widened Z-discs, amorphous sarcomeres, double Z-discs, and supernumerary sarcomeres. We confirm by immunoelectron microscopy that the main Z-disc protein alpha-actinin is not present in Z-disc alterations or in the links of electron-dense material between Z-discs in longitudinal register. These alterations were related to an increase of F-actin and desmin, where F-actin was present within the strands of amorphous material. Desmin, on the other hand, was seen in less dense regions of the alterations. Our results strongly support that the myofibrillar and cytoskeletal alterations, considered to be the hallmarks of DOMS, reflect an adaptive remodeling of the myofibrils.
Similar content being viewed by others
References
Brooks SV, Zerba E, Faulkner JA (1995) Injury to muscle fibers after single stretches of passive and maximally stimulated muscles in mice. J Physiol (Lond) 488:459–469
Carpenter S, Karpati G (2001) Pathology of skeletal muscle, 2nd edn. Oxford University Press, New York
Clarkson PM, Hubal MJ (2002) Exercise-induced muscle damage in humans. Am J Phys Med Rehabil 81:S52–S69
Engel AG, Banker BQ (1994) Ultrastructural changes in diseased muscle. In: Engel AG, Franzini-Armstrong C (eds) Myology, 2nd edn. McGraw-Hill, New York, pp 889–1017
Feasson L, Stockholm D, Freyssenet D, Richard I, Duguez S, Beckmann JS, Denis C (2002) Molecular adaptations of neuromuscular disease-associated proteins in response to eccentric exercise in human skeletal muscle. J Physiol 543:297–306
Friden J (1984) Changes in human skeletal muscle induced by long-term eccentric exercise. Cell Tissue Res 236:365–372
Friden J, Sjostrom M, Ekblom B (1983) Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med 4:170–176
Friden J, Seger J, Ekblom B (1988) Sublethal muscle fibre injuries after high-tension anaerobic exercise. Eur J Appl Physiol 57:360–368
Gibala MJ, MacDougall JD, Tarnopolsky MA, Stauber WT, Elorriaga A (1995) Changes in human skeletal muscle ultrastructure and force production after acute resistance exercise. J Appl Physiol 78:702–708
Lieber RL, Friden J (2002) Mechanisms of muscle injury gleaned from animal models. Am J Phys Med Rehabil 81:S70–S79
Lieber RL, Woodburn TM, Friden J (1991) Muscle damage induced by eccentric contractions of 25% strain. J Appl Physiol 70:2498–2507
McHugh MP (2003) Recent advances in the understanding of the repeated bout effect: the protective effect against muscle damage from a single bout of eccentric exercise. Scand J Med Sci Sports 13:88–97
Morton DJ (1973) Z-line streaming in mammalian muscle fibers. In: Kakulas BA (ed) Basic research in myology, Experta Medica, Amsterdam, pp 483–492
Newham DJ, McPhail G, Mills KR, Edwards RH (1983) Ultrastructural changes after concentric and eccentric contractions of human muscle. J Neurol Sci 61:109–122
Nurenberg P, Giddings CJ, Stray-Gundersen J, Fleckenstein JL, Gonyea WJ, Peshock RM (1992) MR imaging-guided muscle biopsy for correlation of increased signal intensity with ultrastructural change and delayed-onset muscle soreness after exercise. Radiology 184:865–869
Ogilvie RW, Armstrong RB, Baird KE, Bottoms CL (1988) Lesions in the rat soleus muscle following eccentrically biased exercise. Am J Anat 182:335–346
Roth SM, Martel GF, Rogers MA (2000a) Muscle biopsy and muscle fiber hypercontraction: a brief review. Eur J Appl Physiol 83:239–245
Roth SM, Martel GF, Ivey FM, Lemmer JT, Metter EJ, Hurley BF, Rogers MA (2000b) High-volume, heavy-resistance strength training and muscle damage in young and older women. J Appl Physiol 88:1112–1118
Stupka N, Tarnopolsky MA, Yardley NJ, Phillips SM (2001) Cellular adaptation to repeated eccentric exercise-induced muscle damage. J Appl Physiol 91:1669–1678
Wallgren-Pettersson C, Jasani B, Newman GR, Morris GE, Jones S, Singhrao S, Clarke A, Virtanen I, Holmberg C, Rapola J (1995) Alpha-actinin in nemaline bodies in congenital nemaline myopathy: immunological confirmation by light and electron microscopy. Neuromuscul Disord 5:93–104
Yu JG, Thornell LE (2002) Desmin and actin alterations in human muscles affected by delayed onset muscle soreness: a high resolution immunocytochemical study. Histochem Cell Biol 118:171–179
Yu JG, Malm C, Thornell LE (2002) Eccentric contractions leading to DOMS do not cause loss of desmin nor fibre necrosis in human muscle. Histochem Cell Biol 118:29–34
Yu JG, Furst DO, Thornell LE (2003) The mode of myofibril remodelling in human skeletal muscle affected by DOMS induced by eccentric contractions. Histochem Cell Biol 119:383–393
Acknowledgements
We wish to thank M.G. Price, A.G. Crenshaw, and F. Pedrosa-Domellof for valuable comments on the manuscript, and Mrs. M. Enerstedt for excellent technical assistance. This work was supported by grants from the Swedish National Centre for Research in Sports (79/99m 98/04), the Swedish Research Council (12X-03934), and the Medical Faculty of Umeå University.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yu, JG., Carlsson, L. & Thornell, LE. Evidence for myofibril remodeling as opposed to myofibril damage in human muscles with DOMS: an ultrastructural and immunoelectron microscopic study. Histochem Cell Biol 121, 219–227 (2004). https://doi.org/10.1007/s00418-004-0625-9
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00418-004-0625-9