Expression of rainbow trout glucose transporters GLUT1 and GLUT4 during in vitro muscle cell differentiation and regulation by insulin and IGF-I

Insulin is an important factor for the maintenance of glucose homeostasis, enhancing glucose uptake in its target tissues in a process that has been conserved between fish and mammals. In fish skeletal muscle cells, like in mammals, insulin promotes GLUT4 translocation to the plasma membrane and, consequently, glucose uptake, but its role regulating the expression of glucose transporters in vitro has not been demonstrated to date. Thus, we investigated the expression of GLUT4 and GLUT1 throughout skeletal muscle cell differentiation and their regulation by insulin and IGF-I using a primary culture of trout muscle cells. GLUT4 expression gradually increased during the muscle cell differentiation process, whereas GLUT1 expression remained fairly constant. Insulin and IGF-I similarly increased the mRNA levels of GLUT4 in myoblasts and myotubes. On the other hand, IGF-I appeared to be more potent than insulin in stimulating GLUT1 expression, particularly at the myoblast stage. Therefore, this work provides the first demonstration in nonmammalian vertebrates that insulin and IGF-I may act directly on trout muscle cells to regulate the expression of GLUT4 and GLUT1.

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Dual-specificity phosphatase 4 is upregulated during skeletal muscle atrophy and modulates extracellular signal-regulated kinase activity

AJP Cell Physiology ◽

10.1152/ajpcell.00234.2018 ◽

2019 ◽

Vol 316 (4) ◽

pp. C567-C581 ◽

Cited By ~ 9

Author(s):

Ashley N. Haddock ◽

Sydney A. Labuzan ◽

Amy E. Haynes ◽

Caleb S. Hayes ◽

Karina M. Kakareka ◽

...

Keyword(s):

Skeletal Muscle ◽

Cell Differentiation ◽

Map Kinase ◽

Reporter Gene ◽

Muscle Cell ◽

Muscle Cells ◽

Skeletal Muscle Atrophy ◽

Kinase Signaling ◽

Muscle Cell Differentiation ◽

Map Kinase Signaling

Skeletal muscle atrophy results from disparate physiological conditions, including denervation, corticosteroid treatment, and aging. The purpose of this study was to describe and characterize the function of dual-specificity phosphatase 4 (Dusp4) in skeletal muscle after it was found to be induced in response to neurogenic atrophy. Quantitative PCR and Western blot analysis revealed that Dusp4 is expressed during myoblast proliferation but rapidly disappears as muscle cells differentiate. The Dusp4 regulatory region was cloned and found to contain a conserved E-box element that negatively regulates Dusp4 reporter gene activity in response to myogenic regulatory factor expression. In addition, the proximal 3′-untranslated region of Dusp4 acts in an inhibitory manner to repress reporter gene activity as muscle cells progress through the differentiation process. To determine potential function, Dusp4 was fused with green fluorescent protein, expressed in C2C12 cells, and found to localize to the nucleus of proliferating myoblasts. Furthermore, Dusp4 overexpression delayed C2C12 muscle cell differentiation and resulted in repression of a MAP kinase signaling pathway reporter gene. Ectopic expression of a Dusp4 dominant negative mutant blocked muscle cell differentiation and attenuated MAP kinase signaling by preferentially targeting the ERK1/2 branch, but not the p38 branch, of the MAP kinase signaling cascade in skeletal muscle cells. The findings presented in this study provide the first description of Dusp4 in skeletal muscle and suggest that Dusp4 may play an important role in the regulation of muscle cell differentiation by regulating MAP kinase signaling.

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A novel isoform of MAP4 organises the paraxial microtubule array required for muscle cell differentiation

eLife ◽

10.7554/elife.05697 ◽

2015 ◽

Vol 4 ◽

Cited By ~ 29

Author(s):

Binyam Mogessie ◽

Daniel Roth ◽

Zainab Rahil ◽

Anne Straube

Keyword(s):

Cell Differentiation ◽

Cell Fusion ◽

Muscle Cell ◽

Cell Elongation ◽

Myogenic Differentiation ◽

Muscle Cells ◽

Microtubule Array ◽

Muscle Cell Differentiation ◽

Microtubule Transport

The microtubule cytoskeleton is critical for muscle cell differentiation and undergoes reorganisation into an array of paraxial microtubules, which serves as template for contractile sarcomere formation. In this study, we identify a previously uncharacterised isoform of microtubule-associated protein MAP4, oMAP4, as a microtubule organising factor that is crucial for myogenesis. We show that oMAP4 is expressed upon muscle cell differentiation and is the only MAP4 isoform essential for normal progression of the myogenic differentiation programme. Depletion of oMAP4 impairs cell elongation and cell–cell fusion. Most notably, oMAP4 is required for paraxial microtubule organisation in muscle cells and prevents dynein- and kinesin-driven microtubule–microtubule sliding. Purified oMAP4 aligns dynamic microtubules into antiparallel bundles that withstand motor forces in vitro. We propose a model in which the cooperation of dynein-mediated microtubule transport and oMAP4-mediated zippering of microtubules drives formation of a paraxial microtubule array that provides critical support for the polarisation and elongation of myotubes.

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IGF-I and insulin receptor signal transduction in trout muscle cells

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.00294.2005 ◽

2006 ◽

Vol 290 (6) ◽

pp. R1683-R1690 ◽

Cited By ~ 43

Author(s):

Juan Castillo ◽

Ina Ammendrup-Johnsen ◽

Marta Codina ◽

Isabel Navarro ◽

Joaquim Gutiérrez

Keyword(s):

Skeletal Muscle ◽

Signal Transduction ◽

Primary Cultures ◽

Insulin Receptors ◽

Muscle Cells ◽

Skeletal Muscle Cells ◽

Suitable Model ◽

Igf I ◽

Trout Muscle

In this study, primary cultures of trout skeletal muscle cells were used to investigate the main signal transduction pathways of insulin and IGF-I receptors in rainbow trout muscle. At different stages of in vitro development (myoblasts on day 1, myocytes on day 4, and fully developed myotubes on day 11), we detected in these cells the presence of immunoreactivity against ERK 1/2 MAPK and Akt/PKB proteins, components of the MAPK and the phosphatidylinositol 3-kinase-Akt pathways, respectively, two of the main intracellular transduction pathways for insulin and IGF-I receptors. Both insulin and IGF-I activated both pathways, although the latter provoked higher immunoreactivity of phosphorylated MAPKs and Akt proteins. At every stage, increases in total MAPK immunoreactivity levels were observed when cells were stimulated with IGF-I or insulin, while total Akt immunoreactivity levels changed little under stimulation of peptides. Total Akt and total MAPK levels increased as skeletal muscle cells differentiated in culture. Moreover, when cells were incubated with IGF-I or insulin, MAPK-P immunoreactivity levels showed greater increases over the basal levels on days 1 and 4, with no effect observed on day 11. Although Akt-P immunoreactivity displayed improved responses on days 1 and 4 as well, a stimulatory effect was still observed on day 11. In addition, the present study demonstrates that purified trout insulin receptors possess higher phosphorylative activity per unit of receptor than IGF-I receptors. In conclusion, these results indicate that trout skeletal muscle culture is a suitable model to study the insulin and IGF-I signal transduction molecules and that there is a different regulation of MAPK and Akt pathways depending on the developmental stage of the muscle cells.

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Nano-sized graphene oxide coated nanopillars on microgroove polymer arrays that enhance skeletal muscle cell differentiation

Nano Convergence ◽

10.1186/s40580-021-00291-6 ◽

2021 ◽

Vol 8 (1) ◽

Author(s):

Hye Kyu Choi ◽

Cheol-Hwi Kim ◽

Sang Nam Lee ◽

Tae-Hyung Kim ◽

Byung-Keun Oh

Keyword(s):

Skeletal Muscle ◽

Graphene Oxide ◽

Cell Differentiation ◽

Muscle Cell ◽

Microcontact Printing ◽

Traumatic Injury ◽

Skeletal Muscle Cell ◽

Muscle Cell Differentiation ◽

Cellular Environment

AbstractThe degeneration or loss of skeletal muscles, which can be caused by traumatic injury or disease, impacts most aspects of human activity. Among various techniques reported to regenerate skeletal muscle tissue, controlling the external cellular environment has been proven effective in guiding muscle differentiation. In this study, we report a nano-sized graphene oxide (sGO)-modified nanopillars on microgroove hybrid polymer array (NMPA) that effectively controls skeletal muscle cell differentiation. sGO-coated NMPA (sG-NMPA) were first fabricated by sequential laser interference lithography and microcontact printing methods. To compensate for the low adhesion property of polydimethylsiloxane (PDMS) used in this study, graphene oxide (GO), a proven cytophilic nanomaterial, was further modified. Among various sizes of GO, sGO (< 10 nm) was found to be the most effective not only for coating the surface of the NM structure but also for enhancing the cell adhesion and spreading on the fabricated substrates. Remarkably, owing to the micro-sized line patterns that guide cellular morphology to an elongated shape and because of the presence of sGO-modified nanostructures, mouse myoblast cells (C2C12) were efficiently differentiated into skeletal muscle cells on the hybrid patterns, based on the myosin heavy chain expression levels. Therefore, the developed sGO coated polymeric hybrid pattern arrays can serve as a potential platform for rapid and highly efficient in vitro muscle cell generation.

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The neural tube/notochord complex is necessary for vertebral but not limb and body wall striated muscle differentiation

Development ◽

10.1242/dev.115.3.657 ◽

1992 ◽

Vol 115 (3) ◽

pp. 657-672 ◽

Cited By ~ 47

Author(s):

P.M. Rong ◽

M.A. Teillet ◽

C. Ziller ◽

N.M. Le Douarin

Keyword(s):

Cell Differentiation ◽

Muscle Cell ◽

Neural Tube ◽

Body Wall ◽

Muscle Cells ◽

Avian Embryo ◽

Muscle Cell Differentiation ◽

Cell Commitment ◽

Axial Organs

The aim of this work was to investigate the role played by the axial organs, neural tube and notochord, on the differentiation of muscle cells from the somites in the avian embryo. Two of us have previously shown that neuralectomy and notochordectomy is followed by necrosis of the somites and consecutive absence of vertebrae and of most muscle cells derived from the myotomes while the limbs develop normally with muscles. Here we have focused our attention on muscle cell differentiation by using the 13F4 mAb that recognizes a cytoplasmic antigen specific of all types of muscle cells. We show that differentiation of muscle cells of myotomes can occur in the absence of notochord and neural tube provided that the somites from which they are derived have been in contact with the axial organs for a defined period of time, about 10 hours for the first somites formed at the cervical level, a duration that progressively reduces caudalward (i.e. for thoracic and lumbar somites). Either one or the other of the two axial organs, the neural tube or the notochord can prevent somitic cell death and fulfill the requirements for myotomal muscle cell differentiation. Separation of the neural tube/notochord complex from the somites by a surgical slit on one side of the embryo gave the same results as extirpation of these organs and provided a perfect control on the non-operated side. A striking finding was that limb and body wall muscles, although derived from the somites, differentiated in the absence of the axial organs. However, limb muscles that develop after excision of the neural tube started to degenerate from E10 onward due to lack of innervation. In vitro explantation of somites from different axial levels confirmed and defined precisely the chronology of muscle cell commitment in the myotomes as revealed by the in vivo experiments.

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Early Stimulation and Late Inhibition of Extracellular Signal-Regulated Kinase 1/2 Phosphorylation by IGF-I: A Potential Mechanism Mediating the Switch in IGF-I Action on Skeletal Muscle Cell Differentiation

Endocrinology ◽

10.1210/endo.143.2.8648 ◽

2002 ◽

Vol 143 (2) ◽

pp. 511-516 ◽

Cited By ~ 32

Author(s):

Saleh Adi ◽

Bassam Bin-Abbas ◽

Nan-Yan Wu ◽

Stephen M. Rosenthal

Keyword(s):

Skeletal Muscle ◽

Cell Differentiation ◽

Muscle Cell ◽

Skeletal Muscle Cell ◽

Potential Mechanism ◽

Early Stimulation ◽

Extracellular Signal Regulated Kinase ◽

Muscle Cell Differentiation ◽

Extracellular Signal ◽

Igf I

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Posttranscriptional control of embryonic rat skeletal muscle protein synthesis. Control at the level of translation by endogenous RNA.

The Journal of Cell Biology ◽

10.1083/jcb.107.3.1085 ◽

1988 ◽

Vol 107 (3) ◽

pp. 1085-1098 ◽

Cited By ~ 7

Author(s):

C R Vanderburg ◽

M A Nathanson

Keyword(s):

Skeletal Muscle ◽

Cell Differentiation ◽

Muscle Cell ◽

Translational Control ◽

Muscle Protein ◽

Muscle Protein Synthesis ◽

Skeletal Muscle Protein ◽

Rat Skeletal Muscle ◽

Total Rna ◽

Muscle Cell Differentiation

The onset of muscle cell differentiation is associated with increased transcription of muscle-specific mRNA. Studies from this laboratory using 19-d embryonic rat skeletal muscle, suggest that additional, posttranscriptional controls regulate maturation of muscle tissue via a quantitative effect upon translation, and that the regulatory component may reside within the poly A- RNA pool (Nathanson, M.A., E.W. Bush, and C. Vanderburg. 1986. J. Biol. Chem. 261:1477-1486). To further characterize muscle cell translational control, embryonic and adult total RNA were separated into oligo(dT)cellulose-bound (poly A+) and -unbound (poly A-) pools. Unbound material was subjected to agarose gel electrophoresis to resolve constituents of varying molecular size and mechanically cut into five fractions. Material of each fraction was electroeluted and recovered by precipitation. Equivalent loads of total RNA from 19-20-d embryonic rat skeletal muscle exhibited a 40% translational inhibition in comparison to its adult counterpart. Inhibition was not due to decreased message abundance because embryonic, as well as adult muscle, contained equivalent proportions of poly A+ mRNA. An inhibition assay, based upon the translatability of adult RNA and its inhibition by embryonic poly A- RNA, confirmed that inhibition was associated with a 160-2,000-nt poly A- fraction. Studies on the chemical composition of this fraction confirmed its RNA composition, the absence of ribonucleoprotein, and that its activity was absent from similarly fractionated adult RNA. Rescue of inhibition could be accomplished by addition of extra lysate or mRNA; however, smaller proportions of lysate were required, suggesting a strong interaction of inhibitor and components of the translational apparatus. Additional studies demonstrated that the inhibitor acted at the level of initiation, in a dose-dependent fashion. The present studies confirm the existence of translational control in skeletal muscle and suggest that it operates at the embryonic to adult transition. A model of muscle cell differentiation, based upon transcriptional control at the myoblast level, followed by translational regulation at the level of the postmitotic myoblast and/or myotube, is proposed.

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USP19 deubiquitinating enzyme inhibits muscle cell differentiation by suppressing unfolded-protein response signaling

Molecular Biology of the Cell ◽

10.1091/mbc.e14-06-1129 ◽

2015 ◽

Vol 26 (5) ◽

pp. 913-923 ◽

Cited By ~ 18

Author(s):

Benjamin Wiles ◽

Miao Miao ◽

Erin Coyne ◽

Louise Larose ◽

Andrey V. Cybulsky ◽

...

Keyword(s):

Cell Differentiation ◽

Unfolded Protein Response ◽

Muscle Cell ◽

Deubiquitinating Enzyme ◽

Muscle Cell Differentiation ◽

Unfolded Protein ◽

The Unfolded Protein Response ◽

Protein Response

USP19 deubiquitinating enzyme has two isoforms, cytoplasmic and endoplasmic reticulum (ER) localized. The ER-localized isoform specifically suppresses muscle cell differentiation in vitro and appears to do so by inhibiting the unfolded-protein response that occurs during such differentiation. In vivo, loss of USP19 promotes muscle regeneration following injury.

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