Ontogenesis of muscle and adipose tissues and their interactions in ruminants and other species

Abstract

The lean-to-fat ratio, that is, the relative masses of muscle and adipose tissue, is a criterion for the yield and quality of bovine carcasses and meat. This review describes the interactions between muscle and adipose tissue (AT) that may regulate the dynamic balance between the number and size of muscle v. adipose cells. Muscle and adipose tissue in cattle grow by an increase in the number of cells (hyperplasia), mainly during foetal life. The total number of muscle fibres is set by the end of the second trimester of gestation. By contrast, the number of adipocytes is never set. Number of adipocytes increases mainly before birth until 1 year of age, depending on the anatomical location of the adipose tissue. Hyperplasia concerns brown pre-adipocytes during foetal life and white pre-adipocytes from a few weeks after birth. A decrease in the number of secondary myofibres and an increase in adiposity in lambs born from mothers severely underfed during early pregnancy suggest a balance in the commitment of a common progenitor into the myogenic or adipogenic lineages, or a reciprocal regulation of the commitment of two distinct progenitors. The developmental origin of white adipocytes is a subject of debate. Molecular and histological data suggested a possible transdifferentiation of brown into white adipocytes, but this hypothesis has now been challenged by the characterization of distinct precursor cells for brown and white adipocytes in mice. Increased nutrient storage in fully differentiated muscle fibres and adipocytes, resulting in cell enlargement (hypertrophy), is thought to be the main mechanism, whereby muscle and fat masses increase in growing cattle. Competition or prioritization between adipose and muscle cells for the uptake and metabolism of nutrients is suggested, besides the successive waves of growth of muscle v. adipose tissue, by the inhibited or delayed adipose tissue growth in bovine genotypes exhibiting strong muscular development. This competition or prioritization occurs through cellular signalling pathways and the secretion of proteins by adipose tissue (adipokines) and muscle (myokines), putatively regulating their hypertrophy in a reciprocal manner. Further work on the mechanisms underlying cross-talk between brown or white adipocytes and muscle fibres will help to achieve better understanding as a prerequisite to improving the control of body growth and composition in cattle.

Invited review: Pre- and postnatal adipose tissue development in farm animals: from stem cells to adipocyte physiology

“…Maternal undernutrition during early to mid-gestation (days 28 to 80 of gestation) increased the mass of perirenal adipose tissue in near-term fetuses; undernutrition occurring during late gestation (days 115 until term) had the opposite effect. The increased adiposity induced by early maternal undernutrition was also greater in lambs born from mothers fed to requirement than to appetite in late gestation (Bonnet et al, 2010). On the opposite, maternal overfeeding (approx.…”

“…Contrary to pigs, the first groups of adipocytes in cattle are located around the kidney (perirenal fat depot) and appear at 110 days of gestation (40% of gestation); then, adipocytes are apparent at the intermuscular or subcutaneous level at approximately 180 days of gestation (66% of gestation; Vernon, 1986). Intramuscular fat appears after three months of age in cattle, so that IM fat is generally regarded as the last developing adipose tissue in all species (Bonnet et al, 2010). In bovine, adipose tissues represent 4% to 7% of the live weight at birth (Robelin and Casteilla, 1990).…”

“…Unlike other tissues, adipose tissue mass has considerable capacity to expand throughout life as underlined in studies comparing lean and obese subjects (Hausman et al, 2001;Bonnet et al, 2010). The number of adipocytes is set during adolescence in human (Spalding et al, 2008) or in 100 kg of live weights in bovine with some differences between early and late adipose tissues (Bonnet et al, 2010).…”

“…The number of adipocytes is set during adolescence in human (Spalding et al, 2008) or in 100 kg of live weights in bovine with some differences between early and late adipose tissues (Bonnet et al, 2010). Weight variations in the 20% range over periods of several months/ years, do not modify the total number of fat cells in obese or normo-balanced individuals (Spalding et al, 2008) which suggests the presence of mechanisms preserving tissue homeostasis of an individual.…”

Genomic architecture of histone 3 lysine 27 trimethylation during late ovine skeletal muscle development

“…Tertiary fibres first develop on the secondary fibres by gestation days 62–76, and these contribute to the substantial muscle mass present in large mammals, as there is no net increase in the number of muscle fibres after birth in these animals, unlike in small mammals (Stickland 1978; Bonnet et al . 2010). …”