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Pathophysiology of Exercise-Induced Muscle Damage and Its Structural, Functional, Metabolic, and Clinical Consequences

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Pathophysiology of Exercise-Induced Muscle Damage and Its Structural, Functional, Metabolic, and Clinical Consequences Physiol. Res. 69: 565-598, 2020 https://doi.org/10.33549/physiolres.934371 REVIEW Pathophysiology of Exercise-Induced Muscle Damage and Its Structural, Functional, Metabolic, and Clinical Consequences Andraž STOŽER1, Peter VODOPIVC1,2, Lidija KRIŽANČIĆ BOMBEK1 1Institute of Physiology, Faculty of Medicine, University of Maribor, Maribor, Slovenia, 2General Hospital Murska Sobota, Rakičan, Slovenia Received November 18, 2019 Accepted June 9, 2020 Epub Ahead of Print July 16, 2020 Summary 1. Introduction Extreme or unaccustomed eccentric exercise can cause exercise- induced muscle damage, characterized by structural changes In isometric exercise, the contracting muscle involving sarcomere, cytoskeletal, and membrane damage, with an retains its length while producing force, in concentric increased permeability of sarcolemma for proteins. From exercise it shortens, and in eccentric or stretching a functional point of view, disrupted force transmission, altered exercise, it lengthens (Faulkner 2003). Isometric calcium homeostasis, disruption of excitation-contraction coupling, contractions serve to keep posture and hold loads, as well as metabolic changes bring about loss of strength. concentric contractions initiate movements, while Importantly, the trauma also invokes an inflammatory response eccentric contractions typically stop or decelerate them and clinically presents itself by swelling, decreased range of motion, increased passive tension, soreness, and a transient (Hoppeler 2016). If a person is unaccustomed to a speci- decrease in insulin sensitivity. While being damaging and fic exercise or if it is of greater than normal intensity or influencing heavily the ability to perform repeated bouts of duration, all forms of exercise can cause damage and exercise, changes produced by exercise-induced muscle damage pain. However, exercise-induced muscle damage (EIMD) seem to play a crucial role in myofibrillar adaptation. Additionally, is most often caused by high intensity eccentric exercise eccentric exercise yields greater hypertrophy than isometric or (Proske and Morgan 2001). This is most probably concentric contractions and requires less in terms of metabolic because fewer motor units are recruited during eccentric energy and cardiovascular stress, making it especially suitable for exercise compared with other modes of contraction, the elderly and people with chronic diseases. This review focuses resulting in a greater force per active motor unit and thus on our current knowledge of the mechanisms underlying exercise- greater mechanical stress (Douglas et al. 2017a, Tee et al. induced muscle damage, their dependence on genetic background, 2007). In addition to mechanical stress, metabolic stress as well as their consequences at the structural, functional, could also have a role in EIMD associated with eccentric metabolic, and clinical level. A comprehensive understanding of exercise and is probably mostly responsible for cases of these is a prerequisite for proper inclusion of eccentric training in health promotion, rehabilitation, and performance enhancement. EIMD that occur with lower intensity endurance exercises where eccentric contraction is not the only or Key words predominant mode of contraction, such as cycling and Exercise • Eccentric • Muscle • Damage • Pathophysiology running (Tee et al. 2007). EIMD is characterized by several structural and functional changes at various Corresponding author organizational levels, which are the main topic of this Andraž Stožer, Lidija Križančić Bombek, Institute of Physiology, review. At the cellular level, EIMD encompasses damage Faculty of Medicine, University of Maribor, Taborska ulica 8, of myofibrils and Z-line streaming, membrane damage of SI-2000 Maribor, Slovenia. E-mail: [email protected], T-tubules and sarcoplasmic reticulum, disrupted [email protected] PHYSIOLOGICAL RESEARCH • ISSN 1802-9973 (online) 2020 Institute of Physiology of the Czech Academy of Sciences, Prague, Czech Republic Fax +420 241 062 164, e-mail: [email protected], www.biomed.cas.cz/physiolres 566 Stožer et al. Vol. 69 cytoskeletal organization, as well as changes in the action sarcomere overstretches and this process continues of glucose transport proteins, accompanied by changes in iteratively (Morgan 1990). When the muscle relaxes, substrate levels. At the level of the whole organism, myofilaments in the majority of overstretched sarcomeres an increase in specific muscle proteins can be detected in re-interdigitate, but some fail to do so (Talbot and plasma, whereas clinical examination reveals muscle Morgan 1996). Regions with long sarcomere lengths soreness, swelling, decreased muscle strength and range before an active stretch contain the majority of disrupted of motion (Clarkson and Sayers 1999), as well as altered sarcomeres after the stretch and the disrupted sarcomeres proprioception (Walsh et al. 2004). In preparation for this are longer than the rest. The number of disrupted paper, we performed Pubmed and Embase searches for sarcomeres presumably grows with repeated eccentric review articles using the following combination of contractions (Proske and Morgan 2001). Since myofibrils keywords and operators “(exercise induced OR eccentric are anchored to the membrane via the dystrophin exercise) AND physiology AND muscle AND damage complex (Gao and McNally 2015), overstretching the AND review”. We analyzed in detail all articles dealing sarcomeres can also disrupt the anchoring structures, up with key aforementioned etiopathogenetic events in to a point of membrane damage (Owens et al. 2019). This exercise-induced muscle damage and their main increases plasma membrane permeability and disrupts consequences, ranging from the molecular to the systemic excitation-contraction coupling (ECC) (Macpherson et al. level, and included them in the bibliography. We also 1996). A concise illustration of the crucial events and included further relevant review and research articles their proposed temporal sequence in EIMD is given in from within citation lists. Major, mechanistic, pioneering, Figure 1. and most recent articles were given most weight. 2.2 Calcium homeostasis and impaired excitation- 2. Etiology and pathogenesis of EIMD contraction coupling Membrane damage starts with a disruption of the 2.1 Sarcomere overstretch T-tubule system, which negatively affects ECC. According to our current knowledge, the first However, the fall in tension at this point is still reversible step in the development of EIMD is stretching forcibly with caffeine that directly opens sarcoplasmic reticulum the myofibrils (sarcomeres in series) while they are Ca2+ channels, thereby bypassing the ECC pathway contracting and thus disrupting their structure and (Warren et al. 1993). Later, sarcoplasmic reticulum organization, as first demonstrated by Friden and membrane is affected as well because it is linked to the coworkers studying human muscle biopsies 40 years ago T-tubule system by junctophilins. Mouse studies indicate (Fridén et al. 1981, Proske and Allen 2005, Proske and that these play a pivotal role in the interaction between Morgan 2001). More specifically, due to differences in the dihydropyridine receptors on the T-tubule membrane length-tension relationships between individual and the ryanodine Ca2+ release channels on the sarcomeres, the weakest sarcomeres in a myofibril sarcoplasmic reticulum (Fig. 1) (Corona et al. 2010). experience the largest proportion of length change. The Plasma and sarcoplasmic reticulum membrane damage reason for this might be that their actin-myosin overlap is result in uncontrolled Ca2+ entry into the sarcoplasm, further away from its optimum or their cross-sectional triggering a local injury contracture and raising muscle area is somewhat smaller at that moment than in other passive tension, in addition to a fall in active tension sarcomeres. If the length of the sarcomeres is already on (Allen et al. 2005). Interestingly, the ability of artificially the descending limb of their length-tension curves, as the increased intracellular Ca2+ concentration to cause muscle myofilament overlap decreases further with progressive damage was first demonstrated experimentally by stretch, these sarcomeres become progressively weaker. Duncan already in 1978 (Duncan 1978). In the early 90s, 2+ They lengthen rapidly to a point with no myofilament Duan and coworkers then showed that [Ca ]i actually overlap and therefore no active tension production. On rises in skeletal muscle of laboratory rats after prolonged 2+ the other hand, the tension in passive parallel elements in downhill walking (Duan et al. 1990). Elevated [Ca ]i such “popped” sarcomeres increases and balances the subsequently activates the phospholipase-prostaglandin active tension of adjacent sarcomeres, therefore halting pathway and the calpain proteolytic pathway (Clarkson further lengthening (Proske and Morgan 2001). Upon and Sayers 1999, Huang and Zhu 2016). The activated stretching out the muscle fiber, the next-weakest phospholipase A2 promotes further muscle cell damage 2020 Pathophysiology of Exercise-Induced Muscle Damage 567 Fig. 1. Proposed crucial molecular mechanisms of exercise-induced muscle damage etiopathogenesis, symptoms, and the reparation process. 1) Increased tension in eccentric exercise overstretches some of the weakest sarcomeres beyond their myofilament overlap. Such “popped sarcomeres” are unable to produce active tension, which results in direct loss of strength. Increasing external tension causes
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