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B
1
* Department of Pulmonology, Maastricht University, Maastricht, The Netherlands, and
Department of Pathology, University of Vermont, Burlington, Vermont 05405, USA
1Correspondence: Department of Pathology, University of Vermont, Medical Alumni Building A143, Burlington VT 05405, USA. E-mail: yjanssen{at}zoo.uvm.edu
Muscle wasting is often associated with chronic inflammation. Because
tumor necrosis factor
(TNF-
) has been implicated as a major
mediator of cachexia, its effects on C2C12 myocytes were examined.
TNF-
activated nuclear factor-
B (NF-
B) and interfered with the
expression of muscle proteins in differentiating myoblasts.
Introduction of a mutant form of inhibitory protein
B
(I
B
)
restored myogenic differentiation in myoblasts treated with TNF-
or
interleukin 1ß. Conversely, activation of NF-
B by overexpression
of I
B kinase was sufficient to block myogenesis, illustrating the
causal link between NF-
B activation and inhibition of myogenic
differentiation. The inhibitory effects of TNF-
on myogenic
differentiation were reversible, indicating that the effects of the
cytokine were not due to nonspecific toxicity. Treatment of
differentiated myotubes with TNF-
did not result in a striking loss
of muscle-specific proteins, which shows that myogenesis was
selectively affected in the myoblast stage by TNF-
. An important
finding was that NF-
B was activated to the same extent in
differentiating and differentiated cells, illustrating that once
myocytes have differentiated they become refractory to the effects of
NF-
B activation. These results demonstrate that inflammatory
cytokines may contribute to muscle wasting through the inhibition of
myogenic differentiation via a NF-
B-dependent pathway.Langen,
R. C. J., Schols, A. M. W. J., Kelders,
M. C. J. M., Wouters, E. F. M.,
Janssen-Heininger, Y. M. W. Inflammatory cytokines inhibit
myogenic differentiation through activation of nuclear factor-
B.
Key Words: cachexia muscle wasting TNF-
NF-
B myogenic differentiation
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||||
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