Abstract
During myogenesis, reductions in trophic factor availability signal most myoblasts to fuse, up-regulate the expression of muscle-specific genes, and form myotubes. Those cells failing to differentiate into myotubes initiate apoptosis and rapidly die. At present, the signal-transduction molecules that determine whether myoblasts should differentiate or die are largely unknown. In this report, we describe the cloning and characterization of DALP, a small LIM-only type zinc-finger protein that is induced when the intersegmental muscles (ISMs) of the moth Manduca sexta become committed to die at the end of metamorphosis. Forced expression of death-associated LIM-only protein (DALP) in Drosophila results in skeletal muscle atrophy. Ectopic expression of DALP, or its mammalian ortholog Hic-5, blocks differentiation and induces apoptosis in mouse C(2)C(12) myoblasts. Both of these effects can be overcome by contact with normal myoblasts or by ectopic expression of the muscle-specific transcription factor MyoD. Hic-5 expression is specifically and dramatically induced in normal myoblasts that die after removal of trophic support. Taken together, these data suggest that DALP and Hic-5 act upstream of MyoD and function as phylogenetically conserved "switches" to block muscle differentiation and induce death.
MeSH Terms
Amino Acid Sequence
Animals
Animals, Genetically Modified
Base Sequence
Cell Differentiation
Cell Line
Cytoskeletal Proteins/chemistry,genetics,physiology
DNA-Binding Proteins/chemistry,genetics,physiology
Drosophila
Gene Expression Regulation, Developmental
Humans
Insect Proteins
Intracellular Signaling Peptides and Proteins
LIM Domain Proteins
Mammals
Manduca/genetics,growth & development
Mice
Molecular Sequence Data
Muscle Development
Muscles/cytology
Recombinant Proteins/metabolism
Sequence Alignment
Sequence Homology, Amino Acid
Transcription Factors/chemistry,genetics,physiology
Transcription, Genetic
Transfection
Zinc Fingers
Chemicals
Cytoskeletal Proteins
DALP protein, Manduca sexta
DNA-Binding Proteins
Insect Proteins
Intracellular Signaling Peptides and Proteins
LIM Domain Proteins
Recombinant Proteins
TGFB1I1 protein, human
Tgfb1i1 protein, mouse
Transcription Factors
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Hu Y
Molecular and Cellular Biology Program, University of Massachusetts, Amherst, MA 01003, USA.
Cascone P J
Cheng L
Sun D
Nambu J R
Schwartz L M
References (31)
31 references, click to expand
-
Direct association of pp125FAK with paxillin, the focal adhesion-targeting mechanism of pp125FAK.
J Exp Med. 1995 Oct 1;182(4):1089-99
PMID: 7561682
-
Cloning cell death genes.
Methods Cell Biol. 1995;46:107-38
PMID: 7541882
-
Resistance to apoptosis conferred by Cdk inhibitors during myocyte differentiation.
Science. 1996 Jul 19;273(5273):359-61
PMID: 8662523
-
Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg.
Neuron. 1996 Oct;17(4):627-40
PMID: 8893021
-
pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis.
Genes Dev. 1996 Dec 1;10(23):3051-64
PMID: 8957005
-
Rb functions to inhibit apoptosis during myocyte differentiation.
Cancer Res. 1997 Feb 1;57(3):351-4
PMID: 9012453
-
Induction of senescence-like phenotypes by forced expression of hic-5, which encodes a novel LIM motif protein, in immortalized human fibroblasts.
Mol Cell Biol. 1997 Mar;17(3):1224-35
PMID: 9032249
-
Muscle LIM protein promotes myogenesis by enhancing the activity of MyoD.
Mol Cell Biol. 1997 Aug;17(8):4750-60
PMID: 9234731
-
Programmed cell death during animal development.
Br Med Bull. 1997;53(3):570-90
PMID: 9374038
-
The LIM-domain binding protein Ldb1 and its partner LMO2 act as negative regulators of erythroid differentiation.
Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13707-12
PMID: 9391090
-
LIM protein KyoT2 negatively regulates transcription by association with the RBP-J DNA-binding protein.
Mol Cell Biol. 1998 Jan;18(1):644-54
PMID: 9418910
-
Cell adhesion kinase beta forms a complex with a new member, Hic-5, of proteins localized at focal adhesions.
J Biol Chem. 1998 Jan 9;273(2):1003-14
PMID: 9422762
-
Coordinate regulation of cell cycle and apoptosis during myogenesis.
Prog Cell Cycle Res. 1997;3:53-8
PMID: 9552406
-
LIM domains: multiple roles as adapters and functional modifiers in protein interactions.
Trends Genet. 1998 Apr;14(4):156-62
PMID: 9594664
-
Forced expression of hic-5, a senescence-related gene, potentiates a differentiation process of RCT-1 cells induced by retinoic acid.
Int J Biochem Cell Biol. 1998 Jan;30(1):39-45
PMID: 9597752
-
Identification and characterization of LMO4, an LMO gene with a novel pattern of expression during embryogenesis.
Proc Natl Acad Sci U S A. 1998 Sep 15;95(19):11257-62
PMID: 9736723
-
Interaction of Hic-5, A senescence-related protein, with focal adhesion kinase.
J Biol Chem. 1998 Oct 9;273(41):26516-21
PMID: 9756887
-
An essential role of phosphatidylinositol 3-kinase in myogenic differentiation.
Proc Natl Acad Sci U S A. 1998 Nov 24;95(24):14179-83
PMID: 9826674
-
Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle.
Nature. 1977 Dec 22-29;270(5639):725-7
PMID: 563524
-
MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts.
Science. 1988 Oct 21;242(4877):405-11
PMID: 3175662
-
Gene activation is required for developmentally programmed cell death.
Proc Natl Acad Sci U S A. 1990 Sep;87(17):6594-8
PMID: 2395862
-
Activation of polyubiquitin gene expression during developmentally programmed cell death.
Neuron. 1990 Oct;5(4):411-9
PMID: 2169771
-
Cell death during development of the nervous system.
Annu Rev Neurosci. 1991;14:453-501
PMID: 2031577
-
The encephalomyocarditis virus internal ribosome entry site allows efficient coexpression of two genes from a recombinant provirus in cultured cells and in embryos.
Mol Cell Biol. 1991 Dec;11(12):5848-59
PMID: 1658618
-
Social controls on cell survival and cell death.
Nature. 1992 Apr 2;356(6368):397-400
PMID: 1557121
-
Insect muscle as a model for programmed cell death.
J Neurobiol. 1992 Nov;23(9):1312-26
PMID: 1469390
-
Targeted gene expression as a means of altering cell fates and generating dominant phenotypes.
Development. 1993 Jun;118(2):401-15
PMID: 8223268
-
Characterization of the TGF beta 1-inducible hic-5 gene that encodes a putative novel zinc finger protein and its possible involvement in cellular senescence.
J Biol Chem. 1994 Oct 28;269(43):26767-74
PMID: 7929412
-
The LIM domain is a modular protein-binding interface.
Cell. 1994 Oct 21;79(2):211-9
PMID: 7954790
-
MyoD-induced expression of p21 inhibits cyclin-dependent kinase activity upon myocyte terminal differentiation.
Mol Cell Biol. 1995 Jul;15(7):3823-9
PMID: 7791789
-
A member of the phylogenetically conserved CAD family of transcriptional regulators is dramatically up-regulated during the programmed cell death of skeletal muscle in the tobacco hawkmoth Manduca sexta.
Dev Biol. 1996 Feb 1;173(2):499-509
PMID: 8606008