Drosophila β(Heavy)-spectrin is essential for development and contributes to specific cell fates in the eye

Graham H. Thomas, Daniela C. Zarnescu, Amy E. Juedes, Mark A. Bales, Amy Londergan, Carol C. Korte, Daniel P. Kiehart

Research output: Contribution to journalArticle

59 Scopus citations

Abstract

The spectrin membrane skeleton is a ubiquitous cytoskeletal structure with several cellular roles, including the maintenance of cell integrity, determination of cell shape and as a contributor to cell polarity. We have isolated mutations in the gene encoding β(Heavy)-spectrin in Drosophila, and have named this essential locus karst. karst mutant individuals have a pleiotropic phenotype characterized by extensive larval lethality and, in adult escapers, rough eyes, bent wings, tracheal defects and infertility. Within karst mutant eyes, a significant number of ommatidia specifically lack photoreceptor R7 alongside more complex morphological defects. Immunolocalization of β(Heavy)-spectrin in wild-type eye-antennal and wing imaginal discs reveals that β(Heavy)-spectrin is present in a restricted subdomain of the membrane skeleton that colocalizes with DE-cadherin. We propose a model where normal levels of Sevenless signaling are dependent on tight cell-cell adhesion facilitated by the β(Heavy)-spectrin membrane skeleton. Immunolocalization of β(Heavy)-spectrin in the adult and larval midgut indicates that it is a terminal web protein, but we see no gross morphological defects in the adult apical brush border in karst mutant flies. Rhodamine phalloidin staining of karst mutant ovaries similarly reveals no conspicuous defect in the actin cytoskeleton or cellular morphology in egg chambers. This is in contrast to mutations in α-spectrin, the molecular partner of β(Heavy)-spectrin, which affect cellular structure in both the larval gut and adult ovaries. Our results emphasize the fundamental contribution of the spectrin membrane skeleton to normal development and reveals a critical interplay between the integrity of a cell's membrane skeleton, the structure of cell-cell contacts and cell signaling.

Original languageEnglish (US)
Pages (from-to)2125-2134
Number of pages10
JournalDevelopment
Volume125
Issue number11
StatePublished - Jan 1 1998
Externally publishedYes

    Fingerprint

Keywords

  • Cell adhesion
  • Cell signaling
  • Drosophila
  • Eye
  • Spectrin

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology

Cite this

Thomas, G. H., Zarnescu, D. C., Juedes, A. E., Bales, M. A., Londergan, A., Korte, C. C., & Kiehart, D. P. (1998). Drosophila β(Heavy)-spectrin is essential for development and contributes to specific cell fates in the eye. Development, 125(11), 2125-2134.