Maternal and Paternal Genomes Differentially Affect Myofibre Characteristics and Muscle Weights of Bovine Fetuses at Midgestation

Ruidong Xiang,Gail I Anderson,David L Rutley,Paul L Greenwood,Stefan Hiendleder,Tanja Eindorf,William H Johns,Carolyn J Fitzsimmons,Brian M Burns,Mani Ghanipoor-Samami,Claire T Roberts,Zbigniew A Kruk,Dana A Thomsen,Alejandro Lucia

doi:10.1371/journal.pone.0053402

Ruidong Xiang, Gail I Anderson + Show 12 more

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https://doi.org/10.1371/journal.pone.0053402

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Abstract

Postnatal myofibre characteristics and muscle mass are largely determined during fetal development and may be significantly affected by epigenetic parent-of-origin effects. However, data on such effects in prenatal muscle development that could help understand unexplained variation in postnatal muscle traits are lacking. In a bovine model we studied effects of distinct maternal and paternal genomes, fetal sex, and non-genetic maternal effects on fetal myofibre characteristics and muscle mass. Data from 73 fetuses (Day153, 54% term) of four genetic groups with purebred and reciprocal cross Angus and Brahman genetics were analyzed using general linear models. Parental genomes explained the greatest proportion of variation in myofibre size of Musculus semitendinosus (80–96%) and in absolute and relative weights of M. supraspinatus, M. longissimus dorsi, M. quadriceps femoris and M. semimembranosus (82–89% and 56–93%, respectively). Paternal genome in interaction with maternal genome (P<0.05) explained most genetic variation in cross sectional area (CSA) of fast myotubes (68%), while maternal genome alone explained most genetic variation in CSA of fast myofibres (93%, P<0.01). Furthermore, maternal genome independently (M. semimembranosus, 88%, P<0.0001) or in combination (M. supraspinatus, 82%; M. longissimus dorsi, 93%; M. quadriceps femoris, 86%) with nested maternal weight effect (5–6%, P<0.05), was the predominant source of variation for absolute muscle weights. Effects of paternal genome on muscle mass decreased from thoracic to pelvic limb and accounted for all (M. supraspinatus, 97%, P<0.0001) or most (M. longissimus dorsi, 69%, P<0.0001; M. quadriceps femoris, 54%, P<0.001) genetic variation in relative weights. An interaction between maternal and paternal genomes (P<0.01) and effects of maternal weight (P<0.05) on expression of H19, a master regulator of an imprinted gene network, and negative correlations between H19 expression and fetal muscle mass (P<0.001), suggested imprinted genes and miRNA interference as mechanisms for differential effects of maternal and paternal genomes on fetal muscle.

Highlights

Skeletal muscle accounts for up to half of mammalian body mass [1] and has important functions in metabolic homeostasis [2,3]
Wet weights were determined for M. supraspinatus, M. longissimus dorsi, M. quadriceps femoris and M. semimembranosus
Non-genetic maternal effects of final maternal weight accounted for some variation in absolute weights of M. supraspinatus, M. longissimus dorsi and M. quadriceps femoris (5–6%)

Summary

Introduction

Skeletal muscle accounts for up to half of mammalian body mass [1] and has important functions in metabolic homeostasis [2,3]. It is a major source of endocrine factors, including insulinlike growth factors -I (IGF1) and -II (IGF2), key components of the insulin-like growth factor (IGF) system and growth hormone – IGF axis, which are major regulators of pre- and postnatal muscle development and growth [4,5,6,7]. Myofibres differentiate during late fetal development into type I, type IIA (fast oxidative-glycolytic) and type IIX (fast glycolytic) myofibres [10,11]. Myofibre number is established during fetal development and postnatal skeletal muscle mass is largely determined prenatally [9,12] by the interplay of a complex network of genetic and epigenetic factors [13,14,15,16]

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