Nuclear DNA content variation associated with muscle fiber hypertrophic growth in fishes

Abstract

Muscle fiber hypertrophic growth can lead to an increase in the myonuclear domain (MND), leading to greater diffusion distances within the cytoplasmic volume that each nucleus services. We tested the hypothesis that hypertrophic growth in the white muscle of fishes was associated with increases in the mean DNA content of nuclei, which may be a strategy to offset increasing diffusion constraints. DAPI-stained chicken erythrocytes standards and image analysis were used to estimate nuclear DNA content in erythrocytes and muscle fibers from 17 fish species. Mean diploid (2C) values in fish erythrocytes ranged from 0.78 to 7.2 pg. Erythrocyte 2C values were used to determine ploidy level in muscle tissue of small and large size classes of each species. Within each species, mean muscle fiber diameter was greater in the large size class than the small size class, and MND was significantly greater in larger fibers for 11 of the 17 species. Nuclear DNA content per species in muscle ranged from 2 to 64C. Fiber-size dependent increases in ploidy were observed in nine species, which is consistent with our hypothesis and indicates that endoreduplication is occurring during fiber growth. However, two species exhibited significantly lower ploidy in the larger size class, and the mechanistic basis and potential advantage of this ploidy shift is unclear. These results suggest that increases in ploidy may be a common mechanism to compensate for increases in MND associated with fiber hypertrophy in fishes, although it is likely that other factors also affect ploidy changes that occur in muscle during animal growth.

Muscle fiber structure in an aging long‐lived seabird, the black‐legged kittiwake (Rissa tridactyla)

“…However, in our data, number of nuclei did not increase proportionally to fiber size as evidenced by the fact that MND increased significantly with fiber diameter. This finding is consistent with an increase in the MND of white muscle of fishes as a result of an increase in muscle fiber hypertrophic growth (Jimenez & Kinsey, ).…”

“…Because muscle is a postmitotic tissue, to grow hypertrophically, new nuclei must be drawn into the fiber itself from a population of stem‐like cells, termed satellite cells, which can be found in the basement membrane of each muscle fiber, and which are limited in number throughout the lifespan of an animal (Jimenez & Kinsey, ). Myonuclear domain (MND) is defined as the amount of cytoplasm within a muscle fiber that each nucleus is responsible for servicing (Qaisar & Larsson, ).…”

Endopolyploidy as a potential driver of animal ecology and evolution

“…(); 33, Henderson (); 34, Henke & Pohley (); 35, Itono et al . (); 36, Jimenez & Kinsey (); 37, Jimenez et al . (); 38, Jost & Mameli (); 39, Kiknadze & Istomina (); 40, Kooman & Nair (); 41, Korpelainen et al .…”

The effects of dietary β-guanidinopropionic acid on growth and muscle fiber development in juvenile red porgy, Pagrus pagrus

“…The optical thickness was 1 μm with an estimated nuclear length of 9.0 μm, which was found to be the average nuclear length of 17 teleosts in a study from our lab by Jimenez et al (2012; nuclear length data unpublished).…”

“…This leads to multinucleated fibers where each nucleus serves a volume of cell known as the myonuclear domain (MND) (Landing et al 1974; Hall and Ralston 1989; Jimenez et al 2012), and it is generally accepted that myonuclear content increases during hypertrophy (Enesco and Puddy 1964; Adams et al 1998; Roy et al 1999; Bruusgaard et al 2010; van der Meer et al 2011; Jimenez et al 2012). Changes in myonuclear content have been shown to be influenced by both mechanical loading (McCall et al 1998; Adams et al 1999; Roy et al 1999; Bruusgaard et al 2010) and neural stimulation (Ohira 1989; Schmalbruch et al 2000; Kawano et al 2007; van der Meer et al 2011), suggesting that exercise can alter satellite cell fusion.…”