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

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

Research output: Contribution to journalArticle

59 Citations (Scopus)

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

Fingerprint

Spectrin
Drosophila
Skeleton
Membranes
Ovary
Cell Membrane Structures
Imaginal Discs
Cell Polarity
Mutation
Cell Shape
Cellular Structures
Cadherins
Microvilli
Actin Cytoskeleton
Cell Adhesion
Diptera
Infertility
Ovum
Maintenance
Staining and Labeling

All Science Journal Classification (ASJC) codes

  • Molecular Biology
  • Developmental Biology

Cite this

Thomas, C. M., 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.
Thomas, Claire Madison ; Zarnescu, Daniela C. ; Juedes, Amy E. ; Bales, Mark A. ; Londergan, Amy ; Korte, Carol C. ; Kiehart, Daniel P. / Drosophila β(Heavy)-spectrin is essential for development and contributes to specific cell fates in the eye. In: Development. 1998 ; Vol. 125, No. 11. pp. 2125-2134.
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Thomas, CM, Zarnescu, DC, Juedes, AE, Bales, MA, Londergan, A, Korte, CC & Kiehart, DP 1998, 'Drosophila β(Heavy)-spectrin is essential for development and contributes to specific cell fates in the eye', Development, vol. 125, no. 11, pp. 2125-2134.

Drosophila β(Heavy)-spectrin is essential for development and contributes to specific cell fates in the eye. / Thomas, Claire Madison; Zarnescu, Daniela C.; Juedes, Amy E.; Bales, Mark A.; Londergan, Amy; Korte, Carol C.; Kiehart, Daniel P.

In: Development, Vol. 125, No. 11, 01.01.1998, p. 2125-2134.

Research output: Contribution to journalArticle

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AU - Thomas, Claire Madison

AU - Zarnescu, Daniela C.

AU - Juedes, Amy E.

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AU - Londergan, Amy

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AU - Kiehart, Daniel P.

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Thomas CM, Zarnescu DC, Juedes AE, Bales MA, Londergan A, Korte CC et al. Drosophila β(Heavy)-spectrin is essential for development and contributes to specific cell fates in the eye. Development. 1998 Jan 1;125(11):2125-2134.