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Myogenin Expression, Cell Cycle Withdrawal, And Phenotypic Differentiation Are Temporally Separable Events That Precede Cell Fusion Upon Myogenesis

V. Andrés, K. Walsh
Published 1996 · Biology, Medicine

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During terminal differentiation of skeletal myoblasts, cells fuse to form postmitotic multinucleated myotubes that cannot reinitiate DNA synthesis. Here we investigated the temporal relationships among these events during in vitro differentiation of C2C12 myoblasts. Cells expressing myogenin, a marker for the entry of myoblasts into the differentiation pathway, were detected first during myogenesis, followed by the appearance of mononucleated cells expressing both myogenin and the cell cycle inhibitor p21. Although expression of both proteins was sustained in mitogen-restimulated myocytes, 5- bromodeoxyuridine incorporation experiments in serum-starved cultures revealed that myogenin-positive cells remained capable of replicating DNA. In contrast, subsequent expression of p21 in differentiating myoblasts correlated with the establishment of the postmitotic state. Later during myogenesis, postmitotic (p21-positive) mononucleated myoblasts activated the expression of the muscle structural protein myosin heavy chain, and then fused to form multinucleated myotubes. Thus, despite the asynchrony in the commitment to differentiation, skeletal myogenesis is a highly ordered process of temporally separable events that begins with myogenin expression, followed by p21 induction and cell cycle arrest, then phenotypic differentiation, and finally, cell fusion.
This paper references
10.1016/0092-8674(93)90610-3
The MyoD family and myogenesis: Redundancy, networks, and thresholds
H. Weintraub (1993)
Andr6s and Walsh Ordered Myogenic Program 665 on April 6
(1996)
10.1073/PNAS.74.5.2031
Do myoblasts in vivo withdraw from the cell cycle? A reexamination.
P. Buckley (1977)
Cell cycle dependence of differentiation in synchronous skeletal muscle myocytes
P. A. Merrifield (1984)
10.1016/0012-1606(82)90003-3
Isolation and characterization of terminally differentiated chicken and rat skeletal muscle myoblasts.
S. F. Konieczny (1982)
10.1126/science.7863329
p53-independent expression of p21Cip1 in muscle and other terminally differentiating cells
S. Parker (1995)
10.1016/S0014-4827(71)80008-3
Developmental changes preceding cell fusion during muscle differentiation in vitro.
D. Yaffe (1971)
10.1038/345813A0
Cell proliferation inhibited by MyoD1 independently of myogenic differentiation
V. Sorrentino (1990)
10.1016/0014-4827(61)90450-5
DNA synthesis and myogenesis.
F. Stockdale (1961)
10.1016/0092-8674(78)90270-2
Commitment, fusion and biochemical differentiation of a myogenic cell line in the absence of DNA synthesis
B. Nadal-Ginard (1978)
10.1083/JCB.95.3.763
Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro
D. Bader (1982)
10.1016/0022-2836(75)90238-7
Activation of myosin synthesis in fusing and mononucleated myoblasts.
C. Emerson (1975)
10.1016/0014-4827(84)90635-9
Expression of myoblast and myocyte antigens in relation to differentiation and the cell cycle.
H. U. Lee (1984)
10.1016/0012-1606(83)90016-7
Reentry into the cell cycle of differentiated skeletal myocytes.
B. Devlin (1983)
10.1126/science.7863328
Inhibition of myogenic differentiation in proliferating myoblasts by cyclin D1-dependent kinase
S. Skapek (1995)
The duration of the terminal G1 of fusing myoblasts
I. R. Konigsberg (1978)
10.1006/DBIO.1994.1226
Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers.
Z. Yablonka-Reuveni (1994)
10.1016/0014-4827(80)90411-5
Influence of environmental factors on the accumulation and differentiation of prefusion G1 lizard myoblasts in vitro.
E. Bayne (1980)
10.1126/science.7863327
Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD
O. Halevy (1995)
10.1128/MCB.6.5.1412
Transcriptional and posttranscriptional control of c-myc during myogenesis: its mRNA remains inducible in differentiated cells and does not suppress the differentiated phenotype.
T. Endo (1986)
10.1038/227680A0
Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4
U. Laemmli (1970)
10.1128/MCB.11.8.4104
Cyclic amplification and selection of targets (CASTing) for the myogenin consensus binding site.
W. Wright (1991)
10.1016/0012-1606(77)90174-9
Detection of myosin in prefusion G0 lizard myoblasts in vitro.
E. Bayne (1977)
10.1083/JCB.52.1.52
A KINETIC ANALYSIS OF MYOGENESIS IN VITRO
M. O'Neill (1972)
10.1016/0012-1606(76)90151-2
Control of myogenesis in vitro by chick embryo extract.
C. Slater (1976)
10.1016/0092-8674(83)90159-9
Reversibility of muscle differentiation in the absence of commitment: Analysis of a myogenic cell line temperature-sensitive for commitment
H. T. Nguyen (1983)
10.1016/S1043-4682(10)80022-4
Proto-oncogenes in the regulatory circuit for myogenesis.
E. Olson (1992)
10.1101/GAD.3.5.628
A gene with homology to the myc similarity region of MyoD1 is expressed during myogenesis and is sufficient to activate the muscle differentiation program.
D. Edmondson (1989)
10.1083/JCB.41.1.188
MITOSIS AND THE PROCESSES OF DIFFERENTIATION OF MYOGENIC CELLS IN VITRO
R. Bischoff (1969)
10.1016/0012-1606(92)90066-P
Interplay between proliferation and differentiation within the myogenic lineage.
E. Olson (1992)
10.1128/MCB.15.7.3823
MyoD-induced expression of p21 inhibits cyclin-dependent kinase activity upon myocyte terminal differentiation.
K. Guo (1995)
10.1016/0168-9525(92)90373-C
Making muscle in mammals.
M. Buckingham (1992)
10.1016/0012-1606(74)90179-1
Myogenic fusion and the duration of the post-mitotic gap (G1).
P. Buckley (1974)
10.1016/0012-1606(78)90109-4
The duration of the terminal G1 of fusing myoblasts.
I. Konigsberg (1978)
10.1083/JCB.3.5.705
AN ANALYSIS OF MYOGENESIS BY THE USE OF FLUORESCENT ANTIMYOSIN
H. Holtzer (1957)
10.1016/S0955-0674(89)80056-0
Muscle cell differentiation.
N. Rosenthal (1989)
10.1177/29.8.6168681
Mithramycin- and 4'-6-diamidino-2-phenylindole (DAPI)-DNA staining for fluorescence microspectrophotometric measurement of DNA in nuclei, plastids, and virus particles.
A. Coleman (1981)
10.1016/0955-0674(94)90046-9
Regulatory mechanisms that coordinate skeletal muscle differentiation and cell cycle withdrawal.
A. Lassar (1994)
Biochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro
B. Bader (1982)
10.1016/0092-8674(95)90039-X
Mice Lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control
C. Deng (1995)
10.1083/JCB.8.2.333
THE DISSOCIABILITY OF DEOXYRIBONUCLEIC ACID SYNTHESIS FROM THE DEVELOPMENT OF MULTINUCLEARITY OF MUSCLE CELLS IN CULTURE
I. Konigsberg (1960)
Induction of muscle-specific genes in the absence of commitment is reversible
B. Nadal-Ginard (1984)
10.1083/JCB.105.2.949
Growth factor control of skeletal muscle differentiation: commitment to terminal differentiation occurs in G1 phase and is repressed by fibroblast growth factor
C. Clegg (1987)
10.1016/0092-8674(89)90583-7
Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD
W. Wright (1989)
10.1002/JSS.400140407
Control of mouse myoblast commitment to terminal differentiation by mitogens.
T. Linkhart (1980)
10.1146/ANNUREV.PH.53.030191.001221
Hormones, growth factors, and myogenic differentiation.
J. Florini (1991)
Mice lacking p21 ctm/wAH undergo normal development, but are defective in G 1 checkpoint control
C. Deng (1995)
10.1016/0955-0674(90)90157-A
Myogenesis and developmental control genes.
C. Emerson (1990)
Andr6s and Walsh Ordered Myogenic Program
10.1101/GAD.8.1.1
bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out.
E. Olson (1994)
10.1073/PNAS.87.21.8442
MyoD induces growth arrest independent of differentiation in normal and transformed cells.
M. Crescenzi (1990)
10.1016/0012-1606(92)90067-Q
Contractile protein isoforms in muscle development.
E. Bandman (1992)
10.1083/JCB.116.5.1243
MyoD, myogenin independent differentiation of primordial myoblasts in mouse somites
M. G. Cusella-De Angelis (1992)
10.1126/SCIENCE.1846704
The myoD gene family: nodal point during specification of the muscle cell lineage.
H. Weintraub (1991)
10.1101/GAD.4.4.582
Myogenin resides in the nucleus and acquires high affinity for a conserved enhancer element on heterodimerization.
T. Brennan (1990)



This paper is referenced by
10.1016/j.scr.2015.09.012
Ectopic expression of Msx2 in mammalian myotubes recapitulates aspects of amphibian muscle dedifferentiation.
Atilgan Yilmaz (2015)
10.1371/journal.pone.0071632
Notch Pathway Activation Contributes to Inhibition of C2C12 Myoblast Differentiation by Ethanol
M. Arya (2013)
10.3390/cells9061395
Microtubule Organization in Striated Muscle Cells
R. Becker (2020)
Tristetraprolin Regulation of MyoD mRNA Stability Commits Quiescent Adult Muscle Stem Cells to Myogenesis
Melissa A. Hausburg (2010)
10.1042/BSR20160036
Optimization of an in vitro bioassay to monitor growth and formation of myotubes in real time
S. Murphy (2016)
10.1038/cr.2009.39
Globular adiponectin induces differentiation and fusion of skeletal muscle cells
T. Fiaschi (2009)
10.3791/52802
Isolation and Characterization of Satellite Cells from Rat Head Branchiomeric Muscles
P. L. Carvajal Monroy (2015)
10.1083/jcb.200312007
Muscle satellite cells adopt divergent fates
P. Zammit (2004)
10.1111/J.1432-0436.2007.00195.X
Twist induces reversal of myotube formation.
Eleni Hjiantoniou (2008)
10.1016/j.bbrc.2009.12.138
Muscle cells enhance resistance to pro-inflammatory cytokine-induced cartilage destruction.
Dana M Cairns (2010)
10.1083/jcb.200904124
Role of A-type lamins in signaling, transcription, and chromatin organization
V. Andrés (2009)
10.1080/09553000802641177
Protective effects of insulin-like growth factor-I on the decrease in myogenic differentiation by ionizing radiation
T. Sakurai (2009)
10.1016/j.yexcr.2012.06.020
Expression and function of the SDF-1 chemokine receptors CXCR4 and CXCR7 during mouse limb muscle development and regeneration.
Conny Hunger (2012)
10.1038/cdd.2014.189
p53 suppresses muscle differentiation at the myogenin step in response to genotoxic stress
Z. J. Yang (2015)
10.1128/MCB.00550-14
Role of Phosphoinositide 3-OH Kinase p110β in Skeletal Myogenesis
R. W. Matheny (2015)
Tristetraprolin and LPS-inducible CXC chemokine are rapidly induced in presumptive satellite cells in response to skeletal muscle injury.
Chetana Sachidanandan (2002)
Nutrient Requirements Early Posthatch Feeding Stimulates Satellite Cell Proliferation and Skeletal Muscle Growth in Turkey Poults 1
O. Halevy (2003)
10.1002/dvdy.20602
Satellite cells from dystrophic (Mdx) mice display accelerated differentiation in primary cultures and in isolated myofibers
Z. Yablonka-Reuveni (2006)
10.1016/j.msec.2018.07.044
Electroactive biomaterial surface engineering effects on muscle cells differentiation.
S. Ribeiro (2018)
10.1152/ajpheart.1999.277.3.H1100
Vascular smooth muscle cell growth arrest on blockade of thrombospondin-1 requires p21Cip1/WAF1.
D. Chen (1999)
10.1016/S0166-6851(98)00082-6
Host nuclear abnormalities and depletion of nuclear antigens induced in Trichinella spiralis-infected muscle cells by the anthelmintic mebendazole.
C. Yao (1998)
10.20381/RUOR-5327
Six1 Is Important for Myoblast Proliferation Through Direct Regulation of Ccnd1
Ellias Horner (2016)
10.1002/jbm.a.36091
Improving myoblast differentiation on electrospun poly(ε-caprolactone) scaffolds.
Phammela N. Abarzúa-Illanes (2017)
10.1016/j.stemcr.2020.06.004
Induced Fetal Human Muscle Stem Cells with High Therapeutic Potential in a Mouse Muscular Dystrophy Model
M. Zhao (2020)
10.1074/jbc.M509436200
The Amphoterin (HMGB1)/Receptor for Advanced Glycation End Products (RAGE) Pair Modulates Myoblast Proliferation, Apoptosis, Adhesiveness, Migration, and Invasiveness
F. Riuzzi (2006)
10.1083/JCB.135.2.441
Skeletal muscle cells lacking the retinoblastoma protein display defects in muscle gene expression and accumulate in S and G2 phases of the cell cycle
B. Novitch (1996)
10.1128/MCB.19.4.3167
cdk1- and cdk2-Mediated Phosphorylation of MyoD Ser200 in Growing C2 Myoblasts: Role in Modulating MyoD Half-Life and Myogenic Activity
M. Kitzmann (1999)
10.3390/foods9020185
A New Edible Film to Produce In Vitro Meat
N. Orellana (2020)
10.1038/cddis.2017.151
Myogenic differentiation triggers PML nuclear body loss and DAXX relocalization to chromocentres
J. Salsman (2017)
10.1371/journal.pone.0059193
A Rat Model for Muscle Regeneration in the Soft Palate
P. L. Carvajal Monroy (2013)
10.1186/1471-2121-12-26
BMP signaling balances proliferation and differentiation of muscle satellite cell descendants
M. Friedrichs (2010)
10.1111/J.1432-0436.2007.00165.X
Role of eIF3a (eIF3 p170) in intestinal cell differentiation and its association with early development.
Zhaoqian Liu (2007)
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