Myoblasts from intrauterine growth‐restricted sheep fetuses exhibit intrinsic deficiencies in proliferation that contribute to smaller semitendinosus myofibres

Yates, Dustin T; Clarke, Derek S.; Macko, Antoni R.; Anderson, Miranda J.; Shelton, Leslie A.; Nearing, Marie; Allen, Ronald E.; Rhoads, Robert P.; Limesand, Sean W.

doi:10.1113/jphysiol.2014.272591

Cited by 68 publications

(89 citation statements)

References 85 publications

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“…These cells exhibited inappropriate proliferative phenotypes in culture versus aged matched healthy controls (Foulstone et al 2003). Recent studies collectively agree with these findings, confirming muscle derived cells do seem to remember their in vivo environment once isolated from different niches such as type II diabetes (Jiang et al 2013), obesity (Maples and Brault 2015), Please note this is an author accepted version and NOT the final version: The final publication is available at Springer via http://dx.doi.org/10.1007/s10522-015-9604-x intrauterine growth restriction (Yates et al 2014) and low physical activity levels (Green et al 2013;Valencia and Spangenburg 2013).…”

Section: Introductionsupporting

confidence: 70%

“…They collectively suggest muscle derived cells retain a memory once isolated from different environmental niches: (1) muscle derived cells from humans who are physically active, display an improved ability to uptake glucose and are somewhat protected from palmitate induced insulin resistance versus cells isolated from sedentary humans (Green et al 2013;Valencia and Spangenburg 2013); (2) muscle derived cells from obese patients do not respond to lipid oversupply with the same gene expression signatures versus control (Maples and Brault 2015); (3) muscle derived cells from intrauterine growth-restricted sheep fetuses exhibit deficiencies in proliferation versus controls (Yates et al 2014). Importantly all of these studies, highlight that muscle derived stem cells with mitotic potential could be important in the concept of programming/memory in skeletal muscle tissue.…”

Section: Discussionmentioning

confidence: 99%

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Skeletal muscle cells possess a ‘memory’ of acute early life TNF-α exposure: role of epigenetic adaptation

et al. 2015

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Sufficient quantity and quality of skeletal muscle is required to maintain lifespan and healthspan into older age. The concept of skeletal muscle programming or memory has been suggested to contribute to accelerated muscle decline in the elderly in association with early life stress such as fetal malnutrition. Further, muscle cells in vitro appear to remember the in vivo environments from which they are derived (e.g. cancer, obesity, type II diabetes, physical inactivity and nutrient restriction). Tumour-necrosis factor alpha (TNF-α) is a pleiotropic cytokine that is chronically elevated in sarcopenia and cancer cachexia. Higher TNF-α levels are strongly correlated with muscle loss, reduced strength and therefore morbidity and earlier mortality. We have extensively shown that TNF-α impairs regenerative capacity in mouse and human muscle derived stem cells (Meadows 2000;Foulstone 2001Foulstone , 2004Al-Shanti 2008;Saini 2008;Sharples 2010). We have also recently established an epigenetically mediated mechanism (SIRT1-histone deacetylase) regulating survival of myoblasts in the presence of TNF-α (Saini 2012). We therefore wished to extend this work in relation to muscle memory of catabolic stimuli and the potential underlying epigenetic modulation of muscle loss. To enable this aim; C2C12 myoblasts were cultured in the absence or presence of early TNF-α (early proliferative lifespan) followed by 30 population doublings in the absence of TNF-α, prior to the induction of differentiation in low serum media (LSM) in the absence or presence of late TNF-α (late proliferative lifespan). The cells that received an early plus late lifespan dose of TNF-α exhibited reduced morphological (myotube number) and biochemical (creatine kinase activity) differentiation vs. control cells that underwent the same number of proliferative divisions but only a later life encounter with TNF-α. This suggested that muscle cells had a morphological memory of the acute early lifespan TNF-α encounter. Importantly, methylation of myoD CpG islands were increased in the early TNF-α cells, 30 population doublings later, suggesting that even after an acute encounter with TNF-α, the cells have the capability of retaining elevated methylation for at least 30 cellular divisions. Despite these fascinating findings, there were no further increases in myoD methylation or changes in its gene expression when these cells were exposed to a later TNF-α dose suggesting that this was not directly responsible for the decline in differentiation observed. In conclusion, data suggest that elevated myoD methylation is retained throughout muscle cells proliferative lifespan as result of early life TNF-α treatment and has implications for the epigenetic control of muscle loss.

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Section: Introductionsupporting

confidence: 70%

Section: Discussionmentioning

confidence: 99%

Skeletal muscle cells possess a ‘memory’ of acute early life TNF-α exposure: role of epigenetic adaptation

et al. 2015

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“…The rapid progression through these stages of myogenesis may also contribute to the decreased MyoD and myogenin expression in muscle of offspring of obese ewes (Tong et al, 2009), impairing myogenesis during fetal development. Heat stress induced intrauterine growth restriction also resulted in decreased MyoD expression in satellite cells of the offspring after 3 days of culture (Yates et al, 2014). Together, these data demonstrate that the maternal environment has significant impacts on muscle development and satellite cell function, and importantly that in vivo treatments to the animal can alter function in vitro.…”

Section: Discussionmentioning

confidence: 58%

Restricted maternal nutrition alters myogenic regulatory factor expression in satellite cells of ovine offspring

Raja

Hoffman

Govoni

et al. 2016

Animal

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Poor maternal nutrition inhibits muscle development and postnatal muscle growth. Satellite cells are myogenic precursor cells that contribute to postnatal muscle growth, and their activity can be evaluated by the expression of several transcription factors. Pairedbox (Pax)7 is expressed in quiescent and active satellite cells. MyoD is expressed in activated and proliferating satellite cells and myogenin is expressed in terminally differentiating cells. Disruption in the expression pattern or timing of expression of myogenic regulatory factors negatively affects muscle development and growth. We hypothesized that poor maternal nutrition during gestation would alter the in vitro temporal expression of MyoD and myogenin in satellite cells from offspring at birth and 3 months of age. Ewes were fed 100% or 60% of NRC requirements from day 31 ± 1.3 of gestation. Lambs from control-fed (CON) or restricted-fed (RES) ewes were euthanized within 24 h of birth (birth; n = 5) or were fed a control diet until 3 months of age ( n = 5). Satellite cells isolated from the semitendinosus muscle were used for gene expression analysis or cultured for 24, 48 or 72 h and immunostained for Pax7, MyoD or myogenin. Fusion index was calculated from a subset of cells allowed to differentiate. Compared with CON, temporal expression of MyoD and myogenin was altered in cultured satellite cells isolated from RES lambs at birth. The percent of cells expressing MyoD was greater in RES than CON ( P = 0.03) after 24 h in culture. After 48 h of culture, there was a greater percent of cells expressing myogenin in RES compared with CON ( P < 0.001). After 72 h of culture the percent of satellite cells expressing myogenin in RES was less than CON ( P < 0.01). There were no differences in the gene expression of Pax7, Myf5 or MyoD in isolated satellite cells at birth ( P > 0.05). In satellite cells from RES lambs at 3 months of age, the percent of cells expressing MyoD and myogenin were greater than CON after 72 h in culture ( P < 0.05). Fusion index was reduced in RES lambs at 3 months of age compared with CON ( P < 0.001). Restricted nutrition during gestation alters the temporal expression of myogenic regulatory factors in satellite cells of the offspring, which may reduce the pool of myoblasts, decrease myoblast fusion and contribute to the poor postnatal muscle growth previously observed in these animals.

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“…In a variety of species, maternal nutrient restriction during pregnancy limits fetal myoblast cell cycle activity, reduces myonuclei per myofiber, and reduces myofiber number in offspring (Bayol et al, 2004, Costello et al, 2008, Dwyer et al, 1995, Dwyer et al, 1992, Fahey et al, 2005, Greenwood et al, 2000, Greenwood et al, 1999, Osgerby et al, 2002, Prakash et al, 1993, Wilson et al, 1988). Though less well studied, placental insufficiency independent of maternal nutrient intake also results in decreased proliferative capacity of fetal myoblasts, as measured by decreased expression of proliferating cell nuclear antigen (PCNA) and reduced rates of replication in vitro (Yates et al, 2014). …”

Section: The Effects Of Placental Insufficiency On Fetal Skeletal mentioning

confidence: 99%

“…Late gestation fetal and postnatal muscle growth occurs primarily by myofiber hypertrophy (White et al, 2010). Maternal nutrient restriction in sheep, especially towards the end of gestation, reduces myofiber hypertrophy and muscle weights in the fetus (Fahey et al, 2005), as do models of placental insufficiency in guinea pigs and sheep (Bauer et al, 2003, Yates et al, 2014). The AKT-mTORC1 signaling pathway is one of the primary regulators of muscle protein synthesis in response to anabolic stimuli such as amino acids, insulin, and IGF1 in fetal lambs (Anderson et al, 2005, Brown et al, 2009, Shen et al, 2002) as well as in neonatal piglets (O'Connor et al, 2003, O'Connor et al, 2003, Suryawan et al, 2008, Suryawan et al, 2012).…”

Section: The Effects Of Placental Insufficiency On Fetal Skeletal mentioning

confidence: 99%

Impact of placental insufficiency on fetal skeletal muscle growth

Brown

Hay

2016

Molecular and Cellular Endocrinology

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Intrauterine growth restriction (IUGR) caused by placental insufficiency is one of the most common and complex problems in perinatology, with no known cure. In pregnancies affected by placental insufficiency, a poorly functioning placenta restricts nutrient supply to the fetus and prevents normal fetal growth. Among other significant deficits in organ development, the IUGR fetus characteristically has less lean body and skeletal muscle mass than their appropriately-grown counterparts. Reduced skeletal muscle growth is not fully compensated after birth, as individuals who were born small for gestational age (SGA) from IUGR have persistent reductions in muscle mass and strength into adulthood. The consequences of restricted muscle growth and accelerated postnatal “catch-up” growth in the form of adiposity may contribute to the increased later life risk for visceral adiposity, peripheral insulin resistance, diabetes, and cardiovascular disease in individuals who were formerly IUGR. This review will discuss how an insufficient placenta results in impaired fetal skeletal muscle growth and how lifelong reductions in muscle mass might contribute to increased metabolic disease risk in this vulnerable population.

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Myoblasts from intrauterine growth‐restricted sheep fetuses exhibit intrinsic deficiencies in proliferation that contribute to smaller semitendinosus myofibres

Cited by 68 publications

References 85 publications

Skeletal muscle cells possess a ‘memory’ of acute early life TNF-α exposure: role of epigenetic adaptation

Skeletal muscle cells possess a ‘memory’ of acute early life TNF-α exposure: role of epigenetic adaptation

Restricted maternal nutrition alters myogenic regulatory factor expression in satellite cells of ovine offspring

Impact of placental insufficiency on fetal skeletal muscle growth

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