Skeletal muscle as an experimental model of choice to study tissue aging and rejuvenation

Etienne, Jessy; Liu, Chao; Skinner, Colin M.; Conboy, Michael J.; Conboy, Irina M.

doi:10.1186/s13395-020-0222-1

Cited by 38 publications

(31 citation statements)

References 251 publications

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“…In addition to its effects on satellite cells, a dysregulated basal lamina is also expected to disturb the muscle's regenerative capacity through inadequate support of muscle fibers and disorganized scaffold orientation (Sanes, 2003). A review including an extensive summary of the effects of aging on skeletal muscle ECM has recently been published by Etienne et al (2020).…”

Section: Remodeling Of Muscle Ecm With Agingmentioning

confidence: 99%

Skeletal Muscle Extracellular Matrix – What Do We Know About Its Composition, Regulation, and Physiological Roles? A Narrative Review

2020

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Skeletal muscle represents the largest body-composition component in humans. In addition to its primary function in the maintenance of upright posture and the production of movement, it also plays important roles in many other physiological processes, including thermogenesis, metabolism and the secretion of peptides for communication with other tissues. Research attempting to unveil these processes has traditionally focused on muscle fibers, i.e., the contractile muscle cells. However, it is a frequently overlooked fact that muscle fibers reside in a three-dimensional scaffolding that consists of various collagens, glycoproteins, proteoglycans, and elastin, and is commonly referred to as extracellular matrix (ECM). While initially believed to be relatively inert, current research reveals the involvement of ECM cells in numerous important physiological processes. In interaction with other cells, such as fibroblasts or cells of the immune system, the ECM regulates muscle development, growth and repair and is essential for effective muscle contraction and force transmission. Since muscle ECM is highly malleable, its texture and, consequently, physiological roles may be affected by physical training and disuse, aging or various diseases, such as diabetes. With the aim to stimulate increased efforts to study this still poorly understood tissue, this narrative review summarizes the current body of knowledge on (i) the composition and structure of the ECM, (ii) molecular pathways involved in ECM remodeling, (iii) the physiological roles of muscle ECM, (iv) dysregulations of ECM with aging and disease as well as (v) the adaptations of muscle ECM to training and disuse.

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Section: Remodeling Of Muscle Ecm With Agingmentioning

confidence: 99%

Skeletal Muscle Extracellular Matrix – What Do We Know About Its Composition, Regulation, and Physiological Roles? A Narrative Review

2020

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“…Muscular connective tissue changes with advancing age, as reported also in studies in animal models. In particular, its thickness and the amount of collagen cross-linking increase, and its elasticity decreases (Alnaqeeb et al, 1984;Gosselin et al, 1998;Ducomps et al, 2003;Wilke et al, 2019;Etienne et al, 2020). Additionally, the composition of the muscular connective tissue varies; as an example, the amount of collagen type IV rises, and that of type VI reduces (Etienne et al, 2020;Levi et al, 2020).…”

Section: Connective Tissue and Agingmentioning

confidence: 99%

“…In particular, its thickness and the amount of collagen cross-linking increase, and its elasticity decreases (Alnaqeeb et al, 1984;Gosselin et al, 1998;Ducomps et al, 2003;Wilke et al, 2019;Etienne et al, 2020). Additionally, the composition of the muscular connective tissue varies; as an example, the amount of collagen type IV rises, and that of type VI reduces (Etienne et al, 2020;Levi et al, 2020). As a result, the extracellular matrix becomes more rigid and muscles increase their stiffness, thus resulting in impaired muscle function (Alnaqeeb et al, 1984;Kovanen et al, 1984;Gosselin et al, 1998;Willems et al, 2001;Ducomps et al, 2003;Etienne et al, 2020).…”

Section: Connective Tissue and Agingmentioning

confidence: 99%

“…Indeed, experimental evidence from studies in both humans and animal models suggests that aging is associated with a reduction in satellite cell self-renewal and myogenic competences, and possibly a decrease in their number, thus resulting in an impaired regeneration of skeletal muscle tissue ( Corbu et al, 2010 ; Sousa-Victor et al, 2014 ; Brack and Muñoz-Cánoves, 2016 ; Joanisse et al, 2016 ). At the molecular level, aging drives a dysregulation of important molecular signaling pathways, such as FGF2/Sprouty1, Notch, p38 MAPK, JAK-STAT3, and p16(INK4a) in satellite cells, and impairs the microenvironment feeding and regulating the muscle stem cell niche ( Sousa-Victor et al, 2014 ; Parker, 2015 ; Snijders et al, 2015 ; Brack and Muñoz-Cánoves, 2016 ; Joanisse and Parise, 2016 ; Stearns-Reider et al, 2017 ; Etienne et al, 2020 ; Levi et al, 2020 ).…”

Section: Skeletal Muscle and Agingmentioning

confidence: 99%

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Structural and Functional Changes in the Coupling of Fascial Tissue, Skeletal Muscle, and Nerves During Aging

et al. 2020

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Aging is a one-way process associated with profound structural and functional changes in the organism. Indeed, the neuromuscular system undergoes a wide remodeling, which involves muscles, fascia, and the central and peripheral nervous systems. As a result, intrinsic features of tissues, as well as their functional and structural coupling, are affected and a decline in overall physical performance occurs. Evidence from the scientific literature demonstrates that senescence is associated with increased stiffness and reduced elasticity of fascia, as well as loss of skeletal muscle mass, strength, and regenerative potential. The interaction between muscular and fascial structures is also weakened. As for the nervous system, aging leads to motor cortex atrophy, reduced motor cortical excitability, and plasticity, thus leading to accumulation of denervated muscle fibers. As a result, the magnitude of force generated by the neuromuscular apparatus, its transmission along the myofascial chain, joint mobility, and movement coordination are impaired. In this review, we summarize the evidence about the deleterious effect of aging on skeletal muscle, fascial tissue, and the nervous system. In particular, we address the structural and functional changes occurring within and between these tissues and discuss the effect of inflammation in aging. From the clinical perspective, this article outlines promising approaches for analyzing the composition and the viscoelastic properties of skeletal muscle, such as ultrasonography and elastography, which could be applied for a better understanding of musculoskeletal modifications occurring with aging. Moreover, we describe the use of tissue manipulation techniques, such as massage, traction, mobilization as well as acupuncture, dry needling, and nerve block, to enhance fascial repair.

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“…Cells will then migrate from their parent myofiber and attach to the surface of the cell culture dish before undergoing myogenic proliferation and differentiation (Beauchamp et al 2000;Stuelsatz et al 2017). Compared with conventional cell isolation by tissue dissociation, myogenic cultures obtained from single myofibers will have the advantage to be of higher purity (Rosenblatt et al 1995;Etienne et al 2020).…”

Section: Introductionmentioning

confidence: 99%

Isolation and ex vivo cultivation of single myofibers from porcine muscle

Stange

Ahrens²,

Röntgen

2020

In Vitro Cell.Dev.Biol.-Animal

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The isolation and cultivation of intact, single myofibers presents a superior approach for studying myogenic cells in their native position. The cells’ characteristics remain more similar to muscle tissue than in cell culture. Nevertheless, no routinely used method in higher vertebrates exists. Therefore, we aimed at establishing the isolation and cultivation of single myofibers from porcine muscle. For the first time, we implemented the isolation of intact myofibers from porcine fibularis tertius muscle by enzymatic digestion and their subsequent cultivation under floating conditions. Confocal microscopy showed intact myofibrill structures in isolated myofibers. Myogenic cells were able to proliferate at their parent myofiber as shown by the increase of myonuclear number during culture. Additionally, the described method can be used to investigate myogenic cells migrated from isolated myofibers. These cells expressed myogenic markers and were able to differentiate. In the future, our method can be used for genetic manipulation of cells at myofibers, investigation of growth factors or pharmacological substances, and determination of interactions between myofibers and associated cells. Working with isolated myofibers has the potential to bridge conventional cell culture and animal experiments. Adapting the method to porcine muscle allows for application possibilities in veterinary medicine as well as in biomedical research, which cannot be addressed in rodent model systems.

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Skeletal muscle as an experimental model of choice to study tissue aging and rejuvenation

Cited by 38 publications

References 251 publications

Skeletal Muscle Extracellular Matrix – What Do We Know About Its Composition, Regulation, and Physiological Roles? A Narrative Review

Skeletal Muscle Extracellular Matrix – What Do We Know About Its Composition, Regulation, and Physiological Roles? A Narrative Review

Structural and Functional Changes in the Coupling of Fascial Tissue, Skeletal Muscle, and Nerves During Aging

Isolation and ex vivo cultivation of single myofibers from porcine muscle

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