Mechanical Stretch Induces Activation of Skeletal Muscle Satellite Cells in Vitro

doi:10.1006/excr.2001.5252

Experimental Cell Research

Volume 267, Issue 1, 1 July 2001, Pages 107-114

https://doi.org/10.1006/excr.2001.5252 Get rights and content

Abstract

Cultured quiescent satellite cells were subjected to mechanical stretch in a FlexerCell System. In response to stretch, satellite cells entered the cell cycle earlier than if they were under control conditions. Only a brief period of stretch, as short as 2 h, was necessary to stimulate activation. Additionally, conditioned medium from stretched cells could activate unstretched satellite cells. The presence of HGF on c-met-positive myogenic cells was detected by immunofluorescence at 12 h in culture, and immunoblots demonstrated that HGF was released by stretched satellite cells into medium. Also, stretch activation could be abolished by the addition of anti-HGF antibodies to stretched cultures, and activity in conditioned medium from stretched cells could be neutralized by anti-HGF antibodies. In addition, stretch appeared to cause release of preexisting HGF from the extracellular matrix. These experiments suggest that HGF may be involved in linking mechanical perturbation of muscle to satellite cell activation.

References (20)

K.M. McCormick et al.
Mechanisms of nascent fiber formation during avian skeletal muscle hypertrophy
Dev. Biol.
(1992)
R. Tatsumi et al.
HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells
Dev. Biol.
(1998)
R. Bischoff
A satellite cell mitogen from crushed adult muscle
Dev. Biol.
(1986)
D.D.W. Cornelison et al.
Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells
Dev. Biol.
(1997)
C.E. Perrone et al.
Collagen and stretch modulate autocrine secretion of insulin-like growth factor-1 and insulin-like growth factor binding proteins from differentiated skeletal muscle cells
J. Biol. Chem.
(1995)
J.S. Rubin et al.
Hepatocyte growth factor/scatter factor and its receptor, the c-met proto-oncogene product
Biochim. Biophys. Acta Rev. Cancer
(1993)
A. Mauro
Satellite cell of skeletal muscle fibers
J. Biophys. Biochem. Cytol.
(1961)
Bischoff, R.1994. The satellite cell and muscle regeneration. InMyology (A. G. Engel and C. Franzini-Armstrong, Eds.),...
J.M. Kennedy et al.
Nascent muscle fiber appearance in overloaded chicken slow-tonic muscle
Am. J. Anat.
(1988)

There are more references available in the full text version of this article.

Cited by (163)

Decoding the forces that shape muscle stem cell function
2024, Current Topics in Developmental Biology
Skeletal muscle is a force-producing organ composed of muscle tissues, connective tissues, blood vessels, and nerves, all working in synergy to enable movement and provide support to the body. While robust biomechanical descriptions of skeletal muscle force production at the body or tissue level exist, little is known about force application on microstructures within the muscles, such as cells. Among various cell types, skeletal muscle stem cells reside in the muscle tissue environment and play a crucial role in driving the self-repair process when muscle damage occurs. Early evidence indicates that the fate and function of skeletal muscle stem cells are controlled by both biophysical and biochemical factors in their microenvironments, but much remains to accomplish in quantitatively describing the biophysical muscle stem cell microenvironment. This book chapter aims to review current knowledge on the influence of biophysical stresses and landscape properties on muscle stem cells in heath, aging, and diseases.
Lead-free piezoelectric materials for musculoskeletal tissue engineering
2023, Materials Today Sustainability
Musculoskeletal conditions often result in disability and are unfortunately rising in prevalence. Advances in nanotechnology have meant that functional biomaterials are receiving significant interest as implant materials for musculoskeletal tissue engineering. Piezoelectric materials come under the classification of smart materials as they can produce electrical signals in response to mechanical stimuli. The phenomenon is an exciting one within tissue engineering when considering the relevance of bioelectric signals to basic biological processes such as proliferation and differentiation, which ultimately lead to regeneration. In comparison to traditional electrotherapy, possessing innate electrical properties will omit the need for additional power sources, along with associated hassles and safety concerns. Furthermore, given that mechanical loading is a key aspect of musculoskeletal tissue remodeling; we believe piezoelectric material-based scaffolds to be the standout candidate for tissues including bone, cartilage, muscle and so forth. Musculoskeletal conditions are of a global concern and in this review; we specifically focus on the progress of lead-free piezoelectric materials for musculoskeletal tissue engineering purposes. The review also provides an interdisciplinary overview of the fundamentals of piezoelectricity along with a clinical outlook.
Mechanobiology regulation
2023, Multiscale Cell-Biomaterials Interplay in Musculoskeletal Tissue Engineering and Regenerative Medicine
Biophysical stimuli are important for musculoskeletal tissue development and regeneration throughout life. In vitro musculoskeletal tissue engineering strategies have sought to manipulate the biophysical environment, through biomaterial properties and extrinsic mechanical loading, to direct cell activity and tissue formation. However, the extent to which strategies have sought to recreate in vivo processes by which mechanobiological factors govern musculoskeletal tissue development has varied, partly because these processes are not widely understood. This chapter highlights recent advances in understanding of mechanobiology regulation of musculoskeletal tissue regeneration, with a specific focus on mechanosensation mechanisms and biochemical and molecular signaling pathways that govern the mechanobiological responses of musculoskeletal cells in vivo and in vitro. This chapter presents computational studies that have sought to understand the cellular mechanical environment and predict specific tissue regeneration outcomes. A perspective is provided regarding the scientific and technical advancements required to further harness the mechanobiological responses of musculoskeletal cells to develop effective tissue regeneration strategies to treat pathologies.
Obesity impairs skeletal muscle repair through NID-1 mediated extracellular matrix remodeling by mesenchymal progenitors
2022, Matrix Biology
Obesity triggers skeletal muscle physio-pathological alterations. However, the crosstalk between adipose tissue and myogenic cells remains poorly understood during obesity. We identified NID-1 among the adipose tissue secreted factors impairing myogenic potential of human myoblasts and murine muscle stem cells in vitro. Mice under High Fat Diet (HFD) displayed increased NID-1 expression in the skeletal muscle endomysium associated with intramuscular fat adipose tissue expansion and compromised muscle stem cell function. We show that NID-1 is highly secreted by skeletal muscle fibro-adipogenic/mesenchymal progenitors (FAPs) during obesity. We demonstrate that increased muscle NID-1 impairs muscle stem cells proliferation and primes the fibrogenic differentiation of FAPs, giving rise to an excessive deposition of extracellular matrix. Finally, we propose a model in which obesity leads to skeletal muscle extracellular matrix remodeling by FAPs, mediating the alteration of myogenic function by adipose tissue and highlighting the key role of NID-1 in the crosstalk between adipose tissue and skeletal muscle.
A pilot study on nitration/dysfunction of NK1 segment of myogenic stem cell activator HGF
2022, Biochemistry and Biophysics Reports
Protein tyrosine residue (Y) nitration, a post-translational chemical-modification mode, has been associated with changes in protein activity and function; hence the accumulation of specific nitrated proteins in tissues may be used to monitor the onset and progression of pathological disorders. To verify the possible impact of nitration on postnatal muscle growth and regeneration, a pilot study was designed to examine the nitration/dysfunction of hepatocyte growth factor (HGF), a key ligand that is released from the extracellular tethering and activates myogenic stem satellite cells to enter the cell cycle upon muscle stretch and injury. Exposure of recombinant HGF (a hetero-dimer of α- and β-chains) to peroxynitrite induces Y nitration in HGF α-chain under physiological conditions. Physiological significance of this finding was emphasized by Western blotting that showed the NK1 segment of HGF (including a K1 domain critical for signaling-receptor c-met binding) undergoes nitration with a primary target of Y198. Peroxynitrite treatment abolished HGF-agonistic activity of the NK1 segment, as revealed by in vitro c-met binding and bromodeoxyuridine-incorporation assays. Importantly, direct-immunofluorescence microscopy of rat lower hind-limb muscles from two aged-groups (2-month-old “young” and 12-month-old “retired/adult”) provided in vivo evidence for age-related nitration of extracellular HGF (Y198). Overall, findings provide the insight that HGF/NK1 nitration/dysfunction perturbs myogenic stem cell dynamics and homeostasis; hence NK1 nitration may stimulate progression of muscular disorders and diseases including sarcopenia.
Mechano-signaling via Piezo1 prevents activation and p53-mediated senescence of muscle stem cells
2022, Redox Biology
Skeletal muscle stem cells (MuSCs), also called satellite cells, are instrumental for postnatal muscle growth and skeletal muscle regeneration. Numerous signaling cascades regulate the fate of MuSCs during muscle regeneration but the molecular mechanism by which MuSCs sense mechanical stimuli remain unclear. Here, we describe that Piezo1, a mechanosensitive ion channel, keeps MuSCs in a quiescent state and prevents senescence. Absence of Piezo1 induces precocious activation of MuSCs, attenuates proliferation, and impairs differentiation, essentially abolishing efficient skeletal muscle regeneration and replenishment of the MuSC pool. Furthermore, we discovered that inactivation of Piezo1 results in compensatory up-regulation of T-type voltage-gated Ca2+ channels, leading to increased Ca²⁺ influx, which strongly induces NOX4 expression via cPKC. Elevated NOX4 expression in Piezo1-deficient MuSCs increases ROS levels and DNA damage, causing P53-dependent cellular senescence and cell death. The importance of the P53/P21-axis for mediating Piezo1-dependent cellular defects was confirmed by pharmacological inhibition of P53 in Piezo1-deficient mice, which abrogates increased senescence of muscle cells and normalizes muscle regeneration. Our findings uncover an essential role of Piezo1-mediated mechano-signaling in MuSCs for maintaining quiescence and preventing senescence. Reduced mechano-signaling due to decreased physical activity during aging may contribute to the increase of senescent cells and the decline of MuSC numbers in geriatric mice and humans.

View all citing articles on Scopus

¹: To whom reprint requests should be addressed. Fax: (520) 621-1396. E-mail: [email protected].

View full text

Regular ArticleMechanical Stretch Induces Activation of Skeletal Muscle Satellite Cells in Vitro

Abstract

Dev. Biol.

Dev. Biol.

Dev. Biol.

Dev. Biol.

J. Biol. Chem.

Biochim. Biophys. Acta Rev. Cancer

Satellite cell of skeletal muscle fibers

J. Biophys. Biochem. Cytol.

Nascent muscle fiber appearance in overloaded chicken slow-tonic muscle

Am. J. Anat.

Regular Article
Mechanical Stretch Induces Activation of Skeletal Muscle Satellite Cells in Vitro