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PMID:17205126

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Citation

Maqbool, T, Soler, C, Jagla, T, Daczewska, M, Lodha, N, Palliyil, S, VijayRaghavan, K and Jagla, K (2006) Shaping leg muscles in Drosophila: role of ladybird, a conserved regulator of appendicular myogenesis. PLoS ONE 1:e122

Abstract

Legs are locomotor appendages used by a variety of evolutionarily distant vertebrates and invertebrates. The primary biological leg function, locomotion, requires the formation of a specialised appendicular musculature. Here we report evidence that ladybird, an orthologue of the Lbx1 gene recognised as a hallmark of appendicular myogenesis in vertebrates, is expressed in leg myoblasts, and regulates the shape, ultrastructure and functional properties of leg muscles in Drosophila. Ladybird expression is progressively activated in myoblasts associated with the imaginal leg disc and precedes that of the founder cell marker dumbfounded. The RNAi-mediated attenuation of ladybird expression alters properties of developing myotubes, impairing their ability to grow and interact with the internal tendons and epithelial attachment sites. It also affects sarcomeric ultrastructure, resulting in reduced leg muscle performance and impaired mobility in surviving flies. The over-expression of ladybird also results in an abnormal pattern of dorsally located leg muscles, indicating different requirements for ladybird in dorsal versus ventral muscles. This differential effect is consistent with the higher level of Ladybird in ventrally located myoblasts and with positive ladybird regulation by extrinsic Wingless signalling from the ventral epithelium. In addition, ladybird expression correlates with that of FGF receptor Heartless and the read-out of FGF signalling downstream of FGF. FGF signals regulate the number of leg disc associated myoblasts and are able to accelerate myogenic differentiation by activating ladybird, leading to ectopic muscle fibre formation. A key role for ladybird in leg myogenesis is further supported by its capacity to repress vestigial and to down-regulate the vestigial-governed flight muscle developmental programme. Thus in Drosophila like in vertebrates, appendicular muscles develop from a specialised pool of myoblasts expressing ladybird/Lbx1. The ladybird/Lbx1 gene family appears as a part of an ancient genetic circuitry determining leg-specific properties of myoblasts and making an appendage adapted for locomotion.

Links

PubMed PMC1762424 Online version:10.1371/journal.pone.0000122

Keywords

Animals; Animals, Genetically Modified; Biological Evolution; Drosophila/genetics; Drosophila/growth & development; Drosophila/physiology; Drosophila Proteins/antagonists & inhibitors; Drosophila Proteins/genetics; Drosophila Proteins/metabolism; Extremities/growth & development; Female; Fibroblast Growth Factors/metabolism; Gene Expression Regulation, Developmental; Genes, Insect; Homeodomain Proteins/antagonists & inhibitors; Homeodomain Proteins/genetics; Locomotion; Male; Muscle Development/genetics; Muscle Fibers, Skeletal/metabolism; Muscle Fibers, Skeletal/ultrastructure; Muscle Strength; Muscle, Skeletal/growth & development; Myoblasts, Skeletal/metabolism; RNA Interference; Signal Transduction; Transcription Factors/antagonists & inhibitors; Transcription Factors/genetics; Wnt1 Protein/genetics; Wnt1 Protein/metabolism

Significance

Annotations

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

DROME:A0A0B4KH37

involved_in

GO:0007480: imaginal disc-derived leg morphogenesis

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0011278

P

Seeded From UniProt

complete

DROME:A0A0B4KH37

involved_in

GO:0051450: myoblast proliferation

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0011278

P

Seeded From UniProt

complete

DROME:P91626

involved_in

GO:0007480: imaginal disc-derived leg morphogenesis

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0011278

P

Seeded From UniProt

complete

DROME:P91626

involved_in

GO:0051450: myoblast proliferation

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0011278

P

Seeded From UniProt

complete

DROME:Q24416

involved_in

GO:0007480: imaginal disc-derived leg morphogenesis

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0011278

P

Seeded From UniProt

complete

DROME:Q24416

involved_in

GO:0051450: myoblast proliferation

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0011278

P

Seeded From UniProt

complete

DROME:Q4V727

involved_in

GO:0007480: imaginal disc-derived leg morphogenesis

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0011278

P

Seeded From UniProt

complete

DROME:Q4V727

involved_in

GO:0051450: myoblast proliferation

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0011278

P

Seeded From UniProt

complete

DROME:Q61676

involved_in

GO:0007480: imaginal disc-derived leg morphogenesis

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0008651

P

Seeded From UniProt

complete

DROME:Q61676

involved_in

GO:0051450: myoblast proliferation

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0008651

P

Seeded From UniProt

complete

DROME:Q7JMT6

involved_in

GO:0007480: imaginal disc-derived leg morphogenesis

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0008651

P

Seeded From UniProt

complete

DROME:Q7JMT6

involved_in

GO:0051450: myoblast proliferation

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0008651

P

Seeded From UniProt

complete

DROME:Q7KS77

involved_in

GO:0007480: imaginal disc-derived leg morphogenesis

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0008651

P

Seeded From UniProt

complete

DROME:Q7KS77

involved_in

GO:0051450: myoblast proliferation

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0008651

P

Seeded From UniProt

complete

DROME:Q9VDA1

involved_in

GO:0007480: imaginal disc-derived leg morphogenesis

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0008651

P

Seeded From UniProt

complete

DROME:Q9VDA1

involved_in

GO:0051450: myoblast proliferation

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0008651

P

Seeded From UniProt

complete

DROME:Q9VDA2

involved_in

GO:0007480: imaginal disc-derived leg morphogenesis

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0011278

P

Seeded From UniProt

complete

DROME:Q9VDA2

involved_in

GO:0051450: myoblast proliferation

ECO:0000316: genetic interaction evidence used in manual assertion

FB:FBgn0011278

P

Seeded From UniProt

complete


See also

References

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