Matrix metalloproteinase-2 mediates stretch-induced activation of skeletal muscle satellite cells in a nitric oxide-dependent manner

Yamada, Michiko; Sankoda, Yoriko; Tatsumi, Ryuichi; Mizunoya, Wataru; Ikeuchi, Yoshihide; Sunagawa, Kenji; Allen, Ronald E.

doi:10.1016/j.biocel.2008.02.017

Cited by 87 publications

(76 citation statements)

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“…In the regeneration stage, it is believed that MMP-2 is involved in remodeling and maintenance of the ECM. Recent studies indicate that NO upregulates enzymatic activity and protein expression levels of MMP-2 (270) and MMP-9, and this activation of MMP-2 is required for the release of HGF from the ECM upon satellite cell activation (575,576). E) ECM STIFFNESS.…”

Section: Ecm and Associated Factorsmentioning

confidence: 99%

“…Accordingly, iNOS Ϫ/Ϫ mice display delayed satellite cell activation following muscle injury, although injured muscles were still able to regenerate (16). The function of NO-dependent satellite cell activation stems from the ability of NO to promote the release of HGF from the ECM (575,576). MMP-2 was demonstrated to be involved in this process (575).…”

Section: Systemic Milieumentioning

confidence: 99%

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Satellite Cells and the Muscle Stem Cell Niche

Yin

Price

Rudnicki

2013

Physiological Reviews

1,759

1,808

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LYin H, Price F, Rudnicki MA. Satellite Cells and the Muscle Stem Cell Niche. Physiol Rev 93: 23-67, 2013; doi:10.1152/physrev.00043.2011.-Adult skeletal muscle in mammals is a stable tissue under normal circumstances but has remarkable ability to repair after injury. Skeletal muscle regeneration is a highly orchestrated process involving the activation of various cellular and molecular responses. As skeletal muscle stem cells, satellite cells play an indispensible role in this process. The self-renewing proliferation of satellite cells not only maintains the stem cell population but also provides numerous myogenic cells, which proliferate, differentiate, fuse, and lead to new myofiber formation and reconstitution of a functional contractile apparatus. The complex behavior of satellite cells during skeletal muscle regeneration is tightly regulated through the dynamic interplay between intrinsic factors within satellite cells and extrinsic factors constituting the muscle stem cell niche/microenvironment. For the last half century, the advance of molecular biology, cell biology, and genetics has greatly improved our understanding of skeletal muscle biology. Here, we review some recent advances, with focuses on functions of satellite cells and their niche during the process of skeletal muscle regeneration.

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Section: Ecm and Associated Factorsmentioning

confidence: 99%

Section: Systemic Milieumentioning

confidence: 99%

Satellite Cells and the Muscle Stem Cell Niche

Yin

Price

Rudnicki

2013

Physiological Reviews

1,759

1,808

View full text Add to dashboard Cite

show abstract

“…S1A). The cyclic strain protocol was based on literature (Kumar et al, 2004;Yamada et al, 2008) and preliminary data on control myoblasts. It consisted of 10% elongation at 0.5 Hz for 4 h. Just after the completion of the strain, constructs were collected for further experimental procedures.…”

Section: Cyclic Strainmentioning

confidence: 99%

Cellular micro-environments reveal defective mechanosensing responses and elevated YAP signaling in LMNA-mutated muscle precursors

Bertrand

Ziaei

Ehret

et al. 2014

Journal of Cell Science

101

111

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The mechanisms underlying the cell response to mechanical forces are crucial for muscle development and functionality. We aim to determine whether mutations of the LMNA gene (which encodes lamin A/C) causing congenital muscular dystrophy impair the ability of muscle precursors to sense tissue stiffness and to respond to mechanical challenge. We found that LMNA-mutated myoblasts embedded in soft matrix did not align along the gel axis, whereas control myoblasts did. LMNA-mutated myoblasts were unable to tune their cytoskeletal tension to the tissue stiffness as attested by inappropriate cell-matrix adhesion sites and cytoskeletal tension in soft versus rigid substrates or after mechanical challenge. Importantly, in soft two-dimensional (2D) and/or static threedimensional (3D) conditions, LMNA-mutated myoblasts showed enhanced activation of the yes-associated protein (YAP) signaling pathway that was paradoxically reduced after cyclic stretch. siRNAmediated downregulation of YAP reduced adhesion and actin stress fibers in LMNA myoblasts. This is the first demonstration that human myoblasts with LMNA mutations have mechanosensing defects through a YAP-dependent pathway. In addition, our data emphasize the crucial role of biophysical attributes of cellular microenvironment to the response of mechanosensing pathways in LMNA-mutated myoblasts.

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“…The notably acute reduction in SC activation at 21°C versus 27°C may be due to changes in enzyme activity before or after ligand binding to the c-met receptor. However, phosphorylation of matrix metalloproteinase 3, its activity to release HGF from the matrix surrounding fibers (Yamada et al, 2008;Tatsumi and Allen, 2008) and HGF synthesis by the fiber may be susceptible to temperaturedependent regulation. In addition, downstream from HGF-c-met binding, steps in the RAS pathway, subsequent activation of MAPK (Marshall, 1995;O'Brien et al, 2004) or the binding affinity of HGF binding to c-met itself may also be sensitive to lower temperature.…”

Section: Research Articlementioning

confidence: 99%

Satellite cell activation and populations on single muscle-fiber cultures from adult zebrafish (Danio rerio)

Zhang

Anderson

2014

Journal of Experimental Biology

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Satellite cells (SCs), stem cells in skeletal muscle, are mitotically quiescent in adult mammals until activated for growth or regeneration. In mouse muscle, SCs are activated by nitric oxide (NO), hepatocyte growth factor (HGF) and the mechanically induced NO-HGF signaling cascade. Here, the SC population on fibers from the adult, ectothermic zebrafish and SC responsiveness to activating stimuli were assessed using the model system of isolated fibers cultured at 27 and 21°C. SCs were identified by immunostaining for the HGF receptor, c-met, and activation was determined using bromodeoxyuridine uptake in culture or in vivo. In dose-response studies, SC activation was increased by treatment with the NO-donor drug isosorbide dinitrate (1 mmol l −1 ) or HGF (10 ng ml −1 ) to maximum activation at lower concentrations of both than in previous studies of mouse fibers. HGF-induced activation was blocked by anti-c-met antibody, and reduced by culture at 21°C. The effect of cyclical stretch (3 h at 4 cycles per minute) increased activation and was blocked by nitric oxide synthase inhibition and reduced by culture at 21°C. The number of c-met+ SCs per fiber increased rapidly (by 3 h) after stretching. The character of signaling in SC activation on zebrafish fibers, in particular temperature-dependent responses to HGF and stretch, gives new insights into the influence of ectothermy on regulation of muscle growth in teleosts and suggests the use of the single-fiber model system to explore the basis of fiber hyperplasia and the conservation of regulatory pathways between species. KEY WORDS: Stem cells, Ectothermy, Proliferation, c-met, Hepatocyte growth factor INTRODUCTIONSkeletal muscle function in fish is fundamentally important for survival using high-and low-speed swimming (Fauconneau et al., 1995), and the zebrafish [Danio rerio (Hamilton 1822)], an ectothermic teleost, is an important vertebrate model for studying development, physiology and pathology (Lieschke and Currie, 2007). In teleosts, muscle mass [over 90% white fibers (Wakeling and Johnston, 1999)] grows by increases in fiber number and size (Bird and Mabee, 2003;Buckingham and Vincent, 2009). The combination of hyperplasia and hypertrophy is termed indeterminate growth (Fauconneau and Paboeuf, 2001;Rowlerson and Veggetti, 2001;Johnston, 2006), and the growth potential is strongly influenced by temperature (Steinbacher et al., 2011). By comparison, in postnatal mammals, fibers hypertrophy and show accretion of post-mitotic myonuclei, but fibers do not increase in number (Petrella et al., 2008;O'Connor and Pavlath, 2007). Satellite RESEARCH ARTICLEDepartment of Biological Sciences, University of Manitoba, Winnipeg, MB, Canada R3T 2N2. Anderson and Pilipowicz, 2002;Bischoff, 1975;Bischoff, 1986;Bischoff, 1990) and in vivo (Anderson, 2000;Anderson and Wozniak, 2004;Tatsumi and Allen, 2008). Calcium-dependent stretch-activated signals release NO from mechano-sensitive NOS-1μ, which induces HGF release from the extracellular matrix (Tatsumi et al., 2002;Y...

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Matrix metalloproteinase-2 mediates stretch-induced activation of skeletal muscle satellite cells in a nitric oxide-dependent manner

Cited by 87 publications

References 50 publications

Satellite Cells and the Muscle Stem Cell Niche

Satellite Cells and the Muscle Stem Cell Niche

Cellular micro-environments reveal defective mechanosensing responses and elevated YAP signaling in LMNA-mutated muscle precursors

Satellite cell activation and populations on single muscle-fiber cultures from adult zebrafish (Danio rerio)

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