Epidermal tendon cells require Broad Complex function for correct attachment of the indirect flight muscles in Drosophila melanogaster

David J. Sandstrom, Linda L Restifo

Research output: Contribution to journalArticle

14 Citations (Scopus)

Abstract

Drosophila Broad Complex, a primary response gene in the ecdysone cascade, encodes a family of zinc-finger transcription factors essential for metamorphosis. Broad Complex mutations of the rbp complementation group disrupt attachment of the dorsoventral indirect flight muscles during pupal development. We previously demonstrated that isoform BRC-Z1 mediates the muscle attachment function of rbp+ and is expressed in both developing muscle fibers and their epidermal attachment sites. We now report two complementary studies to determine the cellular site and mode of action of rbp+ during maturation of the myotendinous junctions of dorsoventral indirect flight muscles. First, genetic mosaics, produced using the paternal loss method, revealed that the muscle attachment phenotype is determined primarily by the genotype of the dorsal epidermis, with the muscle fiber and the ventral epidermis exerting little or no influence. When the dorsal epidermis was mutant, the vast majority of muscles detached or chose ectopic attachment sites, regardless of the muscle genotype. Conversely, wild-type dorsal epidermis could support attachment of mutant muscles. Second, ultrastructural analysis corroborated and extended these results, revealing defective and delayed differentiation of rbp mutant epidermal tendon cells in the dorsal attachment sites. Tendon cell processes, the stress-bearing links between the epidermis and muscle, were reduced in number and showed delayed appearance of microtubule bundles. In contrast, mutant muscle and ventral epidermis resembled the wild type. In conclusion, BRC-Z1 acts in the dorsal epidermis to ensure differentiation of the myotendinous junction. By analogy with the cell-cell interaction essential for embryonic muscle attachment, we propose that BRC-Z1 regulates one or more components of the epidermal response to a signal from the developing muscle.

Original languageEnglish (US)
Pages (from-to)4051-4065
Number of pages15
JournalJournal of Cell Science
Volume112
Issue number22
StatePublished - 1999

Fingerprint

Drosophila melanogaster
Tendons
Muscles
Epidermis
Genotype
Ecdysone
Zinc Fingers
Cell Communication
Microtubules
Drosophila
Protein Isoforms
Transcription Factors
Phenotype

Keywords

  • Ecdysone cascade
  • Genetic mosaic
  • Metamorphosis
  • Myotendinous junction

ASJC Scopus subject areas

  • Cell Biology

Cite this

Epidermal tendon cells require Broad Complex function for correct attachment of the indirect flight muscles in Drosophila melanogaster. / Sandstrom, David J.; Restifo, Linda L.

In: Journal of Cell Science, Vol. 112, No. 22, 1999, p. 4051-4065.

Research output: Contribution to journalArticle

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