Matrix metalloproteinases are involved in mechanical stretch–induced activation of skeletal muscle satellite cells

Yamada, Michiko; Tatsumi, Ryuichi; Kikuiri, Takashi; Okamoto, Shinpei; Nonoshita, Shinsuke; Mizunoya, Wataru; Ikeuchi, Yoshihide; Shimokawa, Hiroaki; Sunagawa, Kenji; Allen, Ronald E.

doi:10.1002/mus.20601

Cited by 77 publications

(67 citation statements)

References 38 publications

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“…There are many possible roles for MMPs in exercise-induced skeletal muscle remodeling (19,32). In addition to the welldocumented effects of MMPs on angiogenesis, several in vitro studies have shown that the bioavailability of various growth factors is increased by proteolytic cleavage of extracellular matrix molecules and binding proteins (8,9,21).…”

Section: Discussionmentioning

confidence: 99%

Endurance exercise activates matrix metalloproteinases in human skeletal muscle

Rullman¹,

Norrbom²,

Strömberg³

et al. 2009

Journal of Applied Physiology

106

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Section: Discussionmentioning

confidence: 99%

Endurance exercise activates matrix metalloproteinases in human skeletal muscle

Rullman¹,

Norrbom²,

Strömberg³

et al. 2009

Journal of Applied Physiology

106

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“…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;Yamada et al, 2006;Tatsumi et al, 2009;Hara et al, 2012). HGF binds to the c-met receptor on SCs and activation proceeds through p38 mitogen-activated protein kinase and phosphatidyl-inositol 3-kinase pathways (Shi and Garry, 2006).…”

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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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“…Previous studies have suggested that skeletal muscle hypertrophy is accompanied by the activation and contribution of satellite cells, which are released from the muscle fiber basement membrane and typically fuse to the preexisting muscle fibers to contribute to skeletal muscle hypertrophy (Yamada et al, 2006(Yamada et al, , 2008. Many studies have demonstrated that both the MMP-1 (Wang et al, 2009) and the MMP-2 (Zimowska et al, 2008) have important effects on the migration and differentiation of skeletal muscle satellite cells both in in vitro cultured muscle cells and in in vivo animal models, including mdx mice (an X-link dystrophic skeletal muscle mouse model).…”

Section: Discussionmentioning

confidence: 99%

Expression of MMP-1, -2, and -8 in longissimus dorsi muscle and their relationship with meat quality traits in cattle

Qi¹,

Zhang²,

Wang³

et al. 2016

Genet. Mol. Res.

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ABSTRACT. The extracellular matrix (ECM) is the major macromolecule in skeletal muscle, which affects meat quality greatly. The remodeling of the ECM is mainly regulated by matrix metalloproteinases (MMPs). The expression patterns of MMP-1, -2, and -8 in longissimus dorsi muscle were explored using quantitative real-time polymerase chain reaction. The results show that the expression of MMP-1, -2, and -8 decreased significantly from 135 days of pregnancy to postnatal 30 months. While the expression of MMP-1, -2, and -8 showed no significant relationships with intramuscular fat contents, MMP-1 and -2 showed significant negative correlations with the shearing force of the longissimus dorsi muscle in cattle. The expression of MMP-1 also showed a significant negative correlation with cooking loss and a positive correlation with water holding capacity. The expression levels of MMP-1 and -2 were usually higher in fat than in skeletal muscle tissue. The expression of MMP-8 was significantly higher in the mammary fat pad and the longissimus dorsi muscle than in all other tissues. This study indicates that the remodeling of the ECM has important effects both on the development of postnatal skeletal muscle and on meat quality.

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Matrix metalloproteinases are involved in mechanical stretch–induced activation of skeletal muscle satellite cells

Cited by 77 publications

References 38 publications

Endurance exercise activates matrix metalloproteinases in human skeletal muscle

Endurance exercise activates matrix metalloproteinases in human skeletal muscle

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

Expression of MMP-1, -2, and -8 in longissimus dorsi muscle and their relationship with meat quality traits in cattle

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