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PMID:21884692

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Citation

Richard, AF, Demignon, J, Sakakibara, I, Pujol, J, Favier, M, Strochlic, L, Le Grand, F, Sgarioto, N, Guernec, A, Schmitt, A, Cagnard, N, Huang, R, Legay, C, Guillet-Deniau, I and Maire, P (2011) Genesis of muscle fiber-type diversity during mouse embryogenesis relies on Six1 and Six4 gene expression. Dev. Biol. 359:303-20

Abstract

Adult skeletal muscles in vertebrates are composed of different types of myofibers endowed with distinct metabolic and contraction speed properties. Genesis of this fiber-type heterogeneity during development remains poorly known, at least in mammals. Six1 and Six4 homeoproteins of the Six/sine oculis family are expressed throughout muscle development in mice, and Six1 protein is enriched in the nuclei of adult fast-twitch myofibers. Furthermore, Six1/Six4 proteins are known to control the early activation of fast-type muscle genes in myocytes present in the mouse somitic myotome. Using double Six1:Six4 mutants (SixdKO) to dissect in vivo the genesis of muscle fiber-type heterogeneity, we analyzed here the phenotype of the dorsal/epaxial muscles remaining in SixdKO. We show by electron microscopy analysis that the absence of these homeoproteins precludes normal sarcomeric organization of the myofiber leading to a dystrophic aspect, and by immunohistochemistry experiments a deficiency in synaptogenesis. Affymetrix transcriptome analysis of the muscles remaining in E18.5 SixdKO identifies a major role for these homeoproteins in the control of genes that are specifically activated in the adult fast/glycolytic myofibers, particularly those controlling Ca(2+) homeostasis. Absence of Six1 and Six4 leads to the development of dorsal myofibers lacking expression of fast-type muscle genes, and mainly expressing a slow-type muscle program. The absence of restriction of the slow-type program during the fetal period in SixdKO back muscles is associated with a decreased HDAC4 protein level, and subcellular relocalization of the transcription repressor Sox6. Six genes thus behave as essential global regulators of muscle gene expression, as well as a central switch to drive the skeletal muscle fast phenotype during fetal development.

Links

PubMed Online version:10.1016/j.ydbio.2011.08.010

Keywords

Animals; Blotting, Northern; Cells, Cultured; Drosophila Proteins/genetics; Drosophila Proteins/metabolism; Embryo, Mammalian/embryology; Embryo, Mammalian/metabolism; Embryo, Mammalian/ultrastructure; Embryonic Development/genetics; Gene Expression Regulation, Developmental; Homeodomain Proteins/genetics; Homeodomain Proteins/metabolism; Immunohistochemistry; In Situ Hybridization; Mice; Mice, Knockout; Microscopy, Electron, Transmission; Muscle Development/genetics; Muscle Fibers, Fast-Twitch/metabolism; Muscle Fibers, Fast-Twitch/ultrastructure; Muscle Fibers, Skeletal/classification; Muscle Fibers, Skeletal/cytology; Muscle Fibers, Skeletal/metabolism; Muscle Fibers, Slow-Twitch/metabolism; Muscle Fibers, Slow-Twitch/ultrastructure; Myofibrils/metabolism; Myofibrils/ultrastructure; Nerve Tissue Proteins/genetics; Nerve Tissue Proteins/metabolism; Oligonucleotide Array Sequence Analysis; Time Factors; Transcription Factors/genetics; Transcription Factors/metabolism; Transcriptome

Significance

Annotations

Gene product Qualifier GO Term Evidence Code with/from Aspect Extension Notes Status

MOUSE:G3UW82

located_in

GO:0030016: myofibril

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:I6L963

located_in

GO:0030016: myofibril

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:NFM

located_in

GO:0043005: neuron projection

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:SOX6

located_in

GO:0005634: nucleus

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:Q1WNQ9

located_in

GO:0030016: myofibril

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:SIX4

involved_in

GO:0045214: sarcomere organization

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

MOUSE:SIX4

involved_in

GO:0098528: skeletal muscle fiber differentiation

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

MOUSE:SIX4

acts_upstream_of_or_within

GO:0032880: regulation of protein localization

ECO:0000316: genetic interaction evidence used in manual assertion

MGI:MGI:102780

P

Seeded From UniProt

complete

MOUSE:SIX4

acts_upstream_of_or_within

GO:0010468: regulation of gene expression

ECO:0000316: genetic interaction evidence used in manual assertion

MGI:MGI:102780

P

Seeded From UniProt

complete

MOUSE:SIX4

acts_upstream_of_or_within

GO:0008582: regulation of synaptic assembly at neuromuscular junction

ECO:0000316: genetic interaction evidence used in manual assertion

MGI:MGI:102780

P

Seeded From UniProt

complete

MOUSE:SIX1

acts_upstream_of_or_within

GO:0032880: regulation of protein localization

ECO:0000316: genetic interaction evidence used in manual assertion

MGI:MGI:106034

P

Seeded From UniProt

complete

MOUSE:SIX1

acts_upstream_of_or_within

GO:0010468: regulation of gene expression

ECO:0000316: genetic interaction evidence used in manual assertion

MGI:MGI:106034

P

Seeded From UniProt

complete

MOUSE:SIX1

acts_upstream_of_or_within

GO:0008582: regulation of synaptic assembly at neuromuscular junction

ECO:0000316: genetic interaction evidence used in manual assertion

MGI:MGI:106034

P

Seeded From UniProt

complete

MOUSE:SYPH

located_in

GO:0008021: synaptic vesicle

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:ACHA2

located_in

GO:0071944: cell periphery

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:MYH7

located_in

GO:0030016: myofibril

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:Q9WUS5

located_in

GO:0030016: myofibril

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:SYPH

part_of

GO:0008021: synaptic vesicle

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete


See also

References

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