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First published online May 26, 2006
Journal of Experimental Biology 209, 2249-2264 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02153

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Environment and plasticity of myogenesis in teleost fish

Ian A. Johnston

Gatty Marine Laboratory, School of Biology, University of St Andrews, St Andrews, Fife, KY16 8LB, Scotland, UK

View larger version (36K): [in a new window]   Fig. 1. The environmental inputs and physiological systems that affect the functional outputs of skeletal muscle in teleost fish. Altered environmental conditions can result in a behavioural response, i.e. movement to seek a new environment, or lead over time to muscle plasticity, which tunes the functional output of the muscle to the prevailing conditions.

View larger version (30K): [in a new window]   Fig. 2. A model describing the main events of myogenesis in teleost skeletal muscle. In this scheme pleuripotent stems cells become myoblasts, which are committed to a myogenic fate to form the Myogenic Progenitor Cell (MPC) population, involving the expression of the myogenic regulatory factors (MRFs) myoD (myoblast determination factor; there are at least two paralogues in teleosts) and myf-5. Following activation by Hepatocyte Growth Factor/Scatter Factor (HGF/SF) the MPCs are thought to undergo an asymmetric division to regenerate the MPC and provide a daughter cell committed to terminal differentiation. MPC markers (boxed) include c-met (the receptor for HGF/SF), paired-box protein 7 (Pax-7), and the transcription factors, sox-8 and Fox-K1. The MPC progeny undergo a proliferation phase [when proliferating cell nuclear antigen (PCNA), a DNA polymerase associated peptide, is upregulated] controlled by positive and negative signalling pathways. Myostatin-II is an important negative regulator of muscle growth and may also negatively regulate the activation of MPCs (cf. satellite cells in mammals) (McCroskery et al., 2003). Following cell cycle exit (and upregulation of p21), the MPC progeny initiate the differentiation programme involving the expression of the MRFs, myogenin and MRF-4 and MEF-2 gene family members. The MPC progeny can migrate through the muscle and have several fates. Until around 44% of the ultimate fish length, myoblasts in fast muscle can fuse to form short myotubes in a myoblast–myoblast fusion event, which probably involves calpain. Short myotubes can be extended by the fusion of additional myoblasts in a myoblast–myotube fusion event. Once formed myotubes initiate the programme of myofibrillargenesis and mature into muscle fibres. The regulation of fibre mass is thought to be controlled by signalling pathways involving insulin-like growth factor I (IGF-I) and IGF-II. At all stages of growth the MPC progeny can fuse with muscle fibres (myoblast–muscle fibre fusion) in the process of nuclear accretion. As muscle fibres increase in diameter and length additional nuclei are required to maintain the myonuclear domain (the volume of cytoplasm controlled by each nuclei) within certain limits.

View larger version (30K): [in a new window]   Fig. 3. The three phases of myogenesis in the fast myotomal muscle of the arctic charr Salvelinus alpinus: embryonic (blue arrow), stratified hyperplasia (orange arrow) and mosaic hyperplasia (mauve arrow) [based on (Johnston et al., 2004), and D. B. Sibthorpe and I.A.J., unpublished results]. Mosaic hyperplasia is quantitatively the most important phase of myogenesis. In teleosts maternal mRNA transcripts (maternal effects) drive development until the mid-blastula transition when zygotic transcription is initiated. The myoblasts that form the embryonic slow and fast muscle become committed to a myogenic progenitor cell population towards the end of gastrulation, which is much earlier than in amniotes. At least two further phases of myotube production can be distinguished in fast muscle, involving the production of muscle fibres within discrete germinal zones (stratified hyperplasia) and the widespread formation of fibres throughout the myotome (mosaic hyperplasia). (A) The rostral somites of an arctic charr embryo (large benthic morph) at the end of segmentation (751 h.p.f.) illustrating the embryonic phase of myogenesis. The arrows illustrate the intense staining for Pax 7 transcripts in the lateral margin of the myotome extending along the position of the major horizontal septum. The arrowhead shows intense staining in the dorsal region of the spinal cord. (B) Stratified hyperplasia (arrows) in the apical regions of the fast muscle layer of the myotome in an arctic charr juvenile, 4.5 cm fork length. (C) Past evidence of mosaic hyperplasia in the fast muscle of a piscivorous arctic charr morph 35.8 cm fork length. Mature fast fibres (f) are surrounded by daughter fibres at various stages of growth. The fibres labelled (a) and (b) are 14 and 18 µm diameter, respectively. Filled arrowheads represent myonuclei and unfilled arrowheads connective tissue nuclei. Abbreviations: nt, notochord; sc, spinal cord: sk, skin.

View larger version (63K): [in a new window]   Fig. 4. Influence of temperature on the ultrastructure of myotomal muscle in larval Atlantic herring (Clupea harengus) (Vieira and Johnston, 1992). (A) Camera lucida drawing of a 1-day old larva sectioned immediately posterior to the yolk-sac. (B) Transverse electron micrograph of a 1-day old herring larva reared at 12°C. Abbreviations: ds, dermal scale; g, gut; im, embryonic fast muscle fibre; mc, mucocyte; ms, undifferentiated myoblast; mt, mitochondria; my, myofibril; n, myonucleus; nt, notochord; pn, pronephros; SC, spinal cord; sk, skin; sm, embryonic slow muscle fibre. (C,D) The volume density of mitochondria (% fibre volume) in (C) embryonic slow and (D) embryonic fast muscle of 1-day old larvae reared at 5, 10 or 15°C until hatching. Values represent means ± s.e.m., N=20 fibres from 5 larvae per temperature.

View larger version (15K): [in a new window]   Fig. 5. Theoretical reaction norms for myotube production in fast muscle at different temperatures for (A) the embryonic and (B) the stratified hyperplasia stages of myogenesis prior to hatching. (C) The total number of fast muscle fibres per myotomal cross-section present at hatching at the different temperatures. Two reaction norms are illustrated (open and filled circles). In the situation illustrated by the open circles fast fibre number at hatching is apparently independent of temperature, but this is a consequences of the different reaction norms for embryonic and stratified hyperplasia. The norm of reaction illustrated by the filled symbols shows a temperature optimum for myotube production that differs somewhat for the two phases of myogenesis. Note in this example that studying fish reared at just 4 and 12°C and sampled at hatch would result in the erroneous conclusion that muscle fibre production was independent of temperature.

View larger version (13K): [in a new window]   Fig. 6. Myogenin (myog) expression in embryos of the tiger pufferfish (Takifugu rubripes) reared at 15°C (open circles), 18°C (closed circles) and 21°C (closed triangles). The eggs were from a single cross. mRNA transcripts were measured by qPCR using 18S rRNA as an endogenous control. The results were normalised against the highest expression value (21°C, 40 h.p.f.) and plotted against somite interval (development time/divided by the time to form one somite pair) in an attempt to normalise developmental stage at the different temperatures. The results represent mean ± s.e.m. of 4 batches of embryos per temperature. From (Fernandes et al., 2006).

View larger version (33K): [in a new window]   Fig. 7. The recruitment of fast muscle fibres at two temperature regimes in larval herring from hatching until the completion of metamorphosis. Adapted from (Johnston et al., 1998a). The temperature regimes used to rear the larvae are shown in the inset. The cool and warmer temperature regime started at 5°C and 12°C, respectively, and increased during the larval phase. The number of fast muscle fibres per myotomal cross-section for the cool (open circles) and warm (closed circles) are illustrated. The values represent mean ± s.e.m. for 12 larvae per stage/temperature for the first two stages and 6 larvae per temperature/stage for the remaining stages. The relative duration of stratified and mosaic hyperplasia and the morphology of the larvae at three stages is shown.

View larger version (27K): [in a new window]   Fig. 8. Influence of freshwater temperature regime on the recruitment of fast muscle fibres during the seawater stages of Atlantic salmon (Salmo salar L). (A) The number of fast muscle fibres per myotomal cross-section (at the level of the first dorsal fin ray) in relation to fish fork length (cm) during seawater growth. Offspring from a large number of families were reared at cool ambient temperatures or in water heated by 1–3°C during the freshwater stages and then reared together in the same 5 mx5 mx5 m sea cages. The number of fish sampled at each fork length is shown in parentheses. The dotted lines (cool groups, N=45) and the solid lines (heated groups, N=40) represent fish in which fibre recruitment had ceased and these fibre number values represent the maximum (FNmax) for each freshwater treatment. (B) The myonuclei content of isolated fast muscle fibres in relation to fibre diameter (D) for seawater stages of Atlantic salmon. The open circles represent fibres from fish exposed to cool ambient temperatures and the closed circles fish exposed to water heated by 1–3°C during the freshwater stages. Myonuclei content was determined using single fibres stained with the fluorescent DNA stain Sytox GreenTM (Molecular Probes, Leiden, Holland). The lines represent first order linear regressions fitted to the data. The regression equations were as follows: for ambient fish myonuclei=314+17.1D, and for heated fish myonuclei=237+14.3D. See the original publication (Johnston et al., 2003b) for further experimental details.

View larger version (32K): [in a new window]   Fig. 9. The influence of photoperiodic regime on myogenesis in fast muscle of adult seawater stages of Atlantic salmon (Salmo salar L.). (A) The number of fast muscle fibres per myotomal cross-section in fish reared under 24 h continuous light (open circles) or at ambient photoperiod (closed circles). The broken blue line represents sunrise and sunset (Greenwich Mean Time) at Fort William, Scotland where the fish were reared and the green line illustrates daily recordings of sea temperature. The duration of 24 h lighting in the photoperiod manipulated cages is illustrated by the box. The values represent mean ± s.e.m. of 6–12 fish per sample, see original publication for details (Johnston et al., 2003c). (B) The myonuclei content of isolated fast muscle fibres in relation to fibre diameter (D; µm) for the 24 h light-treated fish (open circles) and the ambient day-length fish (closed circles). First-order linear regressions were fitted to the data. For the continuous light-treated fish myonuclei number=1258.1+12.4D (broken line) and for the natural day-length fish myonuclei number=288.6+14.4D (solid line). From (Johnston et al., 2003).